Stem cell ageing and apoptosis

Current Pharmaceutical Design

Volumn 18, Issue 13, 2012, Pages 1694-1717

  Fulle, Stefania ^a   Centurione, Lucia ^a   Mancinelli, Rosa ^a   Sancilio, Silvia ^b   Manzoli, Francesco Antonio ^c   Di Pietro, Roberta ^a  

^a UNIVERSITY OF CHIETI   (Italy)

^b INSTITUTE FOR MATERNAL AND CHILD HEALTH IRCCS BURLO GAROFOLO   (Italy)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

Author keywords

Ageing; Apoptosis; Haematopoietic stem cells; Satellite cells; Self renewal; Stem cells

Indexed keywords

CASPASE 3; CASPASE 7; DEATH RECEPTOR; FAS ASSOCIATED DEATH DOMAIN PROTEIN; MICRORNA; PROTEIN BCL 2; PROTEIN BCL W; PROTEIN BCL X; PROTEIN BCL XL; REACTIVE OXYGEN METABOLITE; RNA BINDING PROTEIN; TELOMERASE REVERSE TRANSCRIPTASE;

APOPTOSIS; CELL AGING; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL METABOLISM; CELL PROLIFERATION; CELL SIZE; CYTOSOL; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DNA STRUCTURE; DNA TEMPLATE; EMBRYO DEVELOPMENT; ENDOPLASMIC RETICULUM; HEMATOPOIETIC STEM CELL; HUMAN; MESENCHYMAL STEM CELL; MUSCLE CELL; NICK END LABELING; NONHUMAN; OOCYTE; OXIDATIVE STRESS; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SATELLITE CELL; SENESCENCE; SIGNAL TRANSDUCTION; SOMATIC CELL; TISSUE REGENERATION; TUMOR SUPPRESSOR GENE;

ADULT; APOPTOSIS; CELL AGING; HUMANS; STEM CELLS;

EID: 84860137513     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/138161212799859657     Document Type: Review

References (380)

1. Phelan JP, Austad SN. Natural selection, dietary restriction, and extended longevity. Growth Dev Aging 1989; 53: 4-6.
2. Medawar PB. An unsolved problem of biology. London, Lewis HK. 1952; 1-24.
3. GC. Pleiotropy, natural selection, and the evolution of senescence. Evolution 1957; 11: 398-411.
4. Kirkwood TB. Evolution of ageing. Nature 1977; 270: 301-304.
5. Sharpless NE, DePinho RA. Telomeres, stem cells, senescence, and cancer. J Clin Invest 2004; 113: 160-168.
6. Rando TA. Stem cells, ageing and the quest for immortality. Nature 2006; 441: 1080-1086.
7. Alenzi FQ, Alenazi BQ, Ahmad SY, Salem ML, Al-Jabri AA, Wyse RK. The haemopoietic stem cell: between apoptosis and self renewal. Yale J Biol Med 2009; 82: 7-18.
8. Weissman IL. Stem cells: units of development, units of regeneration, and units in evolution. Cell 2000; 100: 157-168.
9. Kerr JFR, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26: 239-257.
10. Wyllie AH, Kerr JFR, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68: 251-306.
11. Brouckaert G, Kalai M, Saelens X, Vandenabeele. Apoptotic pathways and their regulation. In: Los M, Gibson SB, Eds. Apoptotic pathways as target for novel therapies in cancer and other diseases. New York, Springer Academic Press 2005; 1-29.
12. Maddika S, Mendoza FJ, Hauff K, Zamzow CR, Paranjothy T, Los M. Cancer-selective therapy of the future: apoptin and its mechanism of action. Cancer Biol Ther 2006; 5: 10-19.
13. Darzynkiewicz Z, Juan G, Li X, Gorczyca W, Murakami T, Tra-ganos F. Cytometry in cell necrobiology: analysis of apoptosis and accidental cell death (necrosis). Cytometry 1997; 27: 1-20.
14. Khosravi-Far R, Esposti MD. Death receptor signals to mitochondria. Cancer Biol Ther 2004; 3: 1051-1057.
15. Di Pietro R, Zauli G. Emerging non-apoptotic functions of Tumor necrosis factor-Related Apoptosis Inducing Ligand (TRAIL)/Apo2L. J Cell Physiol 2004; 201: 331-340.
16. Giampietro F, Sancilio S, Tiboni GM, Rana RA, Di Pietro R. Levels of apoptosis in human granulosa cells seem to be comparable after therapy with a gonadotrophin-releasing hormone agonist or antagonist. Fertil Steril 2006; 85: 412-419.
17. Centurione L, Giampietro F, Sancilio S, et al. Morphometric and ultrastructural analysis of human granulosa cells after gonadotrophin-releasing hormone agonist or antagonist. Reprod Biomed Online 2010; 20: 625-633.
18. Di Giacomo V, Rapino M, Sancilio S, et al. PKC-8 signalling pathway is involved in H9c2 cells differentiation. Differentiation 2010; 80: 204-212.
19. Sancilio S, Di Giacomo V, Quaglietta AM, et al. TRAIL promotes a pro-survival signal in erythropoietin-deprived human erythroblasts through the activation of an NF-kB/IkBci pathway. J Biol Regul Homeost Agents 2011; 25: 375-386.
20. Di Pietro R, Falcieri E, Centurione L, Centurione MA, Mazzotti G, Rana R. Ultrastructural patterns of cell damage and death following gamma radiation exposure of murine erythroleukemia cells. Scanning Microsc 1994; 8: 667-673.
21. Di Pietro R, Centurione L, Santavenere E, et al. Ionizing radiation-induced apoptosis and DNA repair in murine erythroleukemia cells. Scanning Microsc 1996; 10: 253-259.
22. Di Pietro R, Centurione MA, Falcieri E, Centurione L, Santavenere E, Rana R. Dimethylsulfoxide-induced cell death of murine erythroleukemia cells exposed to ionising radiation. Cell Signal 1998; 10: 205-209.
23. Cataldi A, Rapino M, Centurione L, et al. NF-kappaB activation plays an antiapoptotic role in human leukemic K562 cells exposed to ionizing radiation. Cell Biochem 2003; 89: 956-963.
24. Di Pietro R, Centurione L, Sabatini N, et al. Caspase-3 is dually regulated by apoptogenic factors mitochondrial release and by SAPK/JNK metabolic pathway in leukemic cells exposed to etoposide-ionizing radiation combined treatment. Int J Immunopa-thol Pharmacol 2004; 17: 181-190.
25. Sabatini N, Di Pietro R, Rapino M, Sancilio S, Comani S, Cataldi A. PI-3-kinase/NF-kappaB mediated response of Jurkat T leukemic cells to two different chemotherapeutic drugs, etoposide and TRAIL. J Cell Biochem 2004; 93: 301-311.
26. Zauli G, Sancilio S, Cataldi A, Sabatini N, Bosco D, Di Pietro R. PI-3K/Akt and NF-kappaB/IkappaBalpha pathways are activated in Jurkat T cells in response to TRAIL treatment. J Cell Physiol 2005; 202: 900-911.
27. Di Pietro R, Di Giacomo V, Caravatta L, Sancilio S, Rana RA, Cataldi A. Cyclic nucleotide response element binding (CREB) protein activation is involved in K562 erythroleukemia cells differentiation. J Cell Biochem 2007; 100: 1070-1079.
28. Caravatta L, Sancilio S, Di Giacomo V, Rana R, Cataldi A, Di Pietro R. PI3-K/Akt-dependent activation of cAMP-response element-binding (CREB) protein in Jurkat T leukemia cells treated with TRAIL. J Cell Physiol 2008; 214: 192-200.
29. Di Pietro R. Signalling pathways leading to TRAIL resistance. In: InTech Eds, Advances in Cancer Therapy/Book 3, 2011; 201-226.
30. Freitas AA, de Magalhães JP. A review and appraisal of the DNA damage theory of ageing. Mutat Res 2011; 728: 12-22.
31. Kirkwood TB, Austad SN. Why do we age? Nature 2000; 408: 233-238.
32. Mantel C, Broxmeyer HE. Sirtuin 1, stem cells, aging, and stem cell aging. Curr Opin Hematol 2008; 15: 326-331.
33. Holliday R. The multiple and irreversible causes of aging. J Geron-tol A Biol Sci Med Sci 2004; 59: 568-572.
34. Campisi J. Aging, chromatin, and food restriction-connecting the dots. Science 2000; 289: 2062-2063.
35. Bartucci M, Dattilo R, Martinetti D, et al. Prevention of chemotherapy-induced anemia and thrombocytopenia by constant administration of Stem Cell Factor. Clin Cancer Res 2011; 17: 6185-6191.
36. Beltrami AP, Cesselli D, Beltrami CA. At the stem of youth and health. Pharmacol Ther 2011; 129: 3-20.
37. Paradis V, Youssef N, Dargere D, et al. Replicative senescence in normal liver, chronic hepatitis C, and hepatocellular carcinomas. Hum Pathol 2001; 32: 327-332.
38. Going JJ, Stuart RC, Downie M, Fletcher-Monaghan AJ, Keith WN. Senescence-associated beta-galactosidase activity in the upper gastrointestinal tract. J Pathol 2002; 196: 394-400.
39. Campisi J. Senescent cells, tumor suppression, and organismal aging: good citizens, bad neighbors. Cell 2005; 120: 1-10.
40. Sharpless NE, Schatten G. Stem cell aging. J Gerontol A Biol Sci Med Sci 2009; 64: 202-204.
41. Sahin E, Depinho RA. Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 2010; 464: 520-528.
42. Hayflick L, Moorhead PS. The serial cultivation of human diploid cell strains. Exp Cell Res 1961; 25: 585-621.
43. Wynford-Thomas D. Cellular senescence and cancer. J Pathol 1999; 187: 100-111.
44. Sharpless NE, DePinho RA. How stem cells age and why this makes us grow old. Nat Rev Mol Cell Biol 2007; 8: 703-713.
45. Lawless C, Wilkinson DJ, Young A, Addinall SG, Lydall DA. Colonyzer: automated quantification of micro-organism growth characteristics on solid agar. BMC Bioinformatics 2010; 11: 287-299.
46. Ju Z, Zhang J, Gao Y, Cheng T. Telomere dysfunction and cell cycle checkpoints in hematopoietic stem cell aging. Int J Hematol 2011; 94: 33-43.
47. Sherwood SW, Rush D, Ellsworth JL, Schimke RT. Defining cellular senescence in IMR-90 cells: a flow cytometric analysis. Proc Natl Acad Sci USA 1988; 85: 9086-9090.
48. Cristofalo VJ, Pignolo RJ. Replicative senescence of human fibro-blast-like cells in culture. Physiol Rev 1993; 73: 617-638.
49. INK4a. Mol Cell 2004; 14: 501-513.
50. Gonos ES, Derventzi A, Kveiborg M, et al. Cloning and identification of genes that associate with mammalian replicative senescence. Exp Cell Res 1998; 240: 66-74.
51. Pascal T, Debacq-Chainiaux F, Chretien A, et al. Comparison of replicative senescence and stress-induced premature senescence combining differential display and low-density DNA arrays. FEBS Lett 2005; 579: 3651-3659.
52. Blasco MA. Telomere length, stem cells and aging. Nat Chem Biol 2007; 3: 640-649.
53. Blackburn EH. Switching and signaling at the telomere. Cell 2001; 106: 661-673.
54. Passos JF, Saretzki G, von Zglinicki T. DNA damage in telomeres and mitochondria during cellular senescence: is there a connection? Nucleic Acids Res 2007; 35: 7505-7513.
55. Harley CB, Futcher AB, Greider CW. Telomeres shorten during ageing of human fibroblasts. Nature 1990; 345: 458-460.
56. Hastie ND, Dempster M, Dunlop MG, Thompson AM, Green DK, Allshire RC. Telomere reduction in human colorectal carcinoma and with ageing. Nature 1990; 346: 866-868.
57. Allsopp RC, Vaziri H, Patterson C, et al. Telomere length predicts replicative capacity of human fibroblasts. Proc Natl Acad Sci USA 1992; 89: 10114-10118.
58. Deng Y, Chan SS, Chang S. Telomere dysfunction and tumour suppression: the senescence connection. Nat Rev Cancer 2008; 8: 450-458.
59. Martínez P, Blasco MA. Telomeric and extra-telomeric roles for telomerase and the telomere-binding proteins. Nat Rev Cancer 2011; 11: 161-176.
60. Jaskelioff M, Muller FL, Paik JH, et al. Telomerase reactivation reverses tissue degeneration in aged telomerase-deficient mice. Nature 2011; 469: 102-106.
61. Bayreuther K, Rodemann HP, Hommel R, Dittmann K, Albiez M, Francz PI. Human skin fibroblasts in vitro differentiate along a terminal cell lineage. Proc Natl Acad Sci USA 1988; 85: 5112-5116.
62. Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995; 92: 9363-9367.
63. Toussaint O, Dumont P, Dierick JF, et al. Stress-induced premature senescence. Essence of life, evolution, stress, and aging. Ann N Y Acad Sci 2000; 908: 85-98.
64. Robbins E, Levine EM, Eagle H. Morphologic changes accompanying senescence of cultured human diploid cells. J Exp Med 1970; 131: 1211-1222.
65. Brunk U, Ericsson JL, Ponten J, Westermark B. Residual bodies and aging in cultured human glia cells. Effect of entrance into phase 3 and prolonged periods of confluence. Exp Cell Res 1973; 79: 1-14.
66. Gerland LM, Peyrol S, Lallemand C, Branche R, Magaud JP, Ffrench M. Association of increased autophagic inclusions labeled for beta-galactosidase with fibroblastic aging. Exp Gerontol 2003; 38: 887-895.
67. Collado M, Gil J, Efeyan A, et al. Tumour biology: senescence in premalignant tumours. Nature 2005; 436: 642.
68. Narita M, Nunez S, Heard E, et al. Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence. Cell 2003; 113: 703-716.
69. Di Micco R, Cicalese A, Fumagalli M, et al. DNA damage response activation in mouse embryonic fibroblasts undergoing repli-cative senescence and following spontaneous immortalization. Cell Cycle 2008; 7: 3601-3606.
70. Dumont P, Burton M, Chen QM, et al. Induction of replicative senescence biomarkers by sublethal oxidative stresses in normal human fibroblast. Free Radical Biol Med 2000; 28: 361-373.
71. Corral-Debrinski M, Horton T, Lott MT, Shoffner JM, Beal MF, Wallace DC. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Nat Genet 1992; 2: 324-329.
72. Liu VW, Zhang C, Nagley P. Mutations in mitochondrial DNA accumulate differentially in three different human tissues during ageing. Nucleic Acids Res 1998; 26: 1268-1275.
73. Choi HS, Lin Z, Li BS, Liu AY. Age-dependent decrease in the heat-inducible DNA sequence-specific binding activity in human diploid fibroblasts. J Biol Chem 1990; 265: 18005-18011.
74. Blake MJ, Fargnoli J, Gershon D, Holbrook NJ. Concomitant decline in heat-induced hyperthermia and HSP70 mRNA expression in aged rats. Am J Physiol 1991; 260: 663-667.
75. Bitomsky N, Hofmann TG. Apoptosis and autophagy: regulation of apoptosis by DNA damage signalling-roles of p53, p73 and HIPK2. FEBS J 2009; 276: 6074-6083.
76. Dimri GP, Itahana K, Acosta M, Campisi J. Regulation of a senescence checkpoint response by the E2F1 transcription factor and p14 (ARF) tumor suppressor. Mol Cell Biol 2000; 20: 273-285.
77. Condemine W, Takahashi Y, Le Bras M, de Thé H. A nucleolar targeting signal in PML-I addresses PML to nucleolar caps in stressed or senescent cells. J Cell Sci 2007; 120: 3219-3227.
78. Lafferty-Whyte K, Cairney CJ, Jamieson NB, Oien KA, Keith WN. Pathway analysis of senescence-associated miRNA targets reveals common processes to different senescence induction mechanisms. Biochim Biophys Acta 2009; 1792: 341-352.
79. Abdelmohsen K, Pullmann R, Lal A, et al. Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol Cell 2007; 25: 543-557.
80. Jung JW, Lee S, Seo MS, et al. Histone deacetylase controls adult stem cell aging by balancing the expression of polycomb genes and jumonji domain containing 3. Cell Mol Life Sci 2010; 67: 1165-1176.
81. Adams PD. Healing and hurting: molecular mechanisms, functions, and pathologies of cellular senescence. Mol Cell 2009; 36: 2-14.
82. Patschan S, Chen J, Polotskaia A, et al. Lipid mediators of autophagy in stress-induced premature senescence of endothelial cells. Am J Physiol Heart Circ Physiol 2008; 294: 1119-1129.
83. Fukuda D, Sata M. Role of bone marrow renin-angiotensin system in the pathogenesis of atherosclerosis. Pharmacol Ther 2008; 118: 268-276.
84. Orjalo AV, Bhaumik D, Gengler BK, Scott GK, Campisi J. Cell surface-bound IL-1 alpha is an upstream regulator of the senescence-associated IL-6/IL-8 cytokine network. Proc Natl Acad Sci USA 2009; 106: 17031-17036.
85. Pan L, Chen S, Weng C, et al. Stem cell aging is controlled both intrinsically and extrinsically in the Drosophila ovary. Cell Stem Cell 2007; 1: 458-469.
86. Mayack SR, Shadrach JL, Kim FS, Wagers AJ. Systemic signals regulate ageing and rejuvenation of blood stem cell niches. Nature 2010; 463: 495-500.
87. Mendez MV, Stanley A, Phillips T, Murphy M, Menzoian JO, Park HY. Fibroblasts cultured from distal lower extremities in patients with venous reflux display cellular characteristics of senescence. J Vasc Surg 1998; 28: 1040-1050.
88. Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Ko-muro I. Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation 2002; 105: 1541-1544.
89. Price JS, Waters JG, Darrah C, et al. The role of chondrocyte senescence in osteoarthritis. Aging Cell 2002; 1: 57-65.
90. Giacomoni PU, Declercq L, Hellemans L, Maes D. Aging of human skin: review of a mechanistic model and first experimental data. IUBMB Life 2000; 49: 259-263.
91. Murakami S, Tedesco PM, Cypser JR, Johnson TE. Molecular genetic mechanisms of life span manipulation in Caenorhabditis elegans. Ann N Y Acad Sci 2000; 908: 40-49.
92. Lin YJ, Seroude L, Benzer S. Extended life-span and stress resistance in the Drosophila mutant methuselah. Science 1998; 282: 943-946.
93. Salmon AB, Murakami S, Bartke A, Kopchick J, Yasumura K, Miller RA. Fibroblast cell lines from young adult mice of long-lived mutant strains are resistant to multiple forms of stress. Am J Physiol Endocrinol Metab 2005; 289: 23-29.
94. Gebhart E, Bauer R, Raub U, Schinzel M, Ruprecht KW, Jonas JB. Spontaneous and induced chromosomal instability in Werner syndrome. Hum Genet 1988; 80: 135-139.
95. Weismann A. On heredity. Claredon Press, Oxford 1891.
96. Walter CA, Walter RB, McCarrey JR. Germline genomes-a biological fountain of youth? Sci Aging Knowledge Environ 2003; 2003: PE4.
97. Park Y, Gerson SL. DNA repair defects in stem cell function and aging. Annu Rev Med 2005; 56: 495-508.
98. van Loon AA, Sonneveld E, Hoogerbrugge J, et al. Induction and repair of DNA single-strand breaks and DNA base damage at different cellular stages of spermatogenesis of the hamster upon in vitro exposure to ionizing radiation. Mutat Res 1993; 294: 139-148.
99. Medvedev ZA. On the immortality of the germ line: genetic and biochemical mechanism. A review. Mech Ageing Dev 1981; 17: 331-359.
100. Holliday R. The biological significance of meiosis. Symp Soc Exp Biol 1984; 38: 381-394.
101. WR. A means to an end: the biological basis of aging and death. New York, Oxford University Press 1999; 1-234.
102. L. How and why we age. New York, Ballantine Books 1994; 1-377.
103. Liu Y, Sanoff HK, Cho H, et al. Expression of p16(INK4a) in peripheral blood T-cells is a biomarker of human aging. Aging Cell 2009; 8: 439-448.
104. Zhang J, Ju Z. Telomere, DNA damage, and oxidative stress in stem cell aging. Birth Defects Res C Embryo Today 2010; 90: 297-307.
105. Brack AS, Rando TA. Intrinsic changes and extrinsic influences of myogenic stem cell function during aging. Stem Cell Rev 2007; 3: 226-237.
106. Mimeault M, Hauke R, Batra SK. Stem cells: a revolution in therapeutics-recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clin Pharmacol Ther 2007; 82: 252-264.
107. Drummond-Barbosa D. Stem cells, their niches and the systemic environment: an aging network. Genetics 2008; 180: 1787-1797.
108. de Magalhães JP. From cells to ageing: a review of models and mechanisms of cellular senescence and their impact on human ageing. Exp Cell Res 2004; 300: 1-10.
109. Meier JJ, Lin JC, Butler AE, Galasso R, Martinez DS, Butler PC. Direct evidence of attempted (3 cell regeneration in an 89-year-old patient with recent-onset type 1 diabetes. Diabetologia 2006; 49: 1838-1844.
110. Krishnamurthy J, Ramsey MR, Ligon KL, et al. p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 2006; 443: 453-457.
111. Zhang X, Ebata KT, Robaire B, Nagano MC. Aging of male germ line stem cells in mice. Biol Reprod 2006; 74: 119-124.
112. Martin K, Potten CS, Roberts SA, Kirkwood TB. Altered stem cell regeneration in irradiated intestinal crypts of senescent mice. J Cell Sci 1998; 111: 2297-2303.
113. Geiger H, Van Zant G. The aging of lympho-hematopoietic stem cells. Nat Immunol 2002; 3: 329-333.
114. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003; 302: 1575-1577.
115. Hattiangady B, Shetty AK. Implications of decreased hippocampal neurogenesis in chronic temporal lobe epilepsy. Epilepsia 2008; 49: 26-41.
116. Vaziri H, Dragowska W, Allsopp RC, Thomas TE, Harley CB, Lansdorp PM. Evidence for a mitotic clock in human hema-topoietic stem cells: loss of telomeric DNA with age. Proc Natl Acad Sci USA 1994; 91: 9857-9860.
117. Rossi DJ, Bryder D, Zahn JM, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 2005; 102: 9194-9199.
118. Carlson ME, Conboy MJ, Hsu M, et al. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 2009; 8: 676-689.
119. Selesniemi K, Lee HJ, Niikura T, Tilly JL. Young adult donor bone marrow infusions into female mice postpone age-related reproductive failure and improve offspring survival. Aging 2009; 11: 49-57.
120. Lymperi S, Ferraro F, Scadden DT. The HSC niche concept has turned 31. Has our knowledge matured? Ann N Y Acad Sci 2010; 1192: 12-18.
121. Rossi DJ, Bryder D, Seita J, Nussenzweig A, Hoeijmakers J, Weissman IL. Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 2007; 447: 725-729.
122. Chen TL. Inhibition of growth and differentiation of osteoprogeni-tors in mouse bone marrow stromal cell cultures by increased donor age and glucocorticoid treatment. Bone 2004; 35: 83-95.
123. Conboy IM, Conboy MJ, Wagers AJ, Girma ER, Weissman IL, Rando TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005; 433: 760-764.
124. Jacobson MD, Weil M, Raff MC. Programmed cell death in animal development. Cell 1997; 88: 347-354.
125. Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995: 267: 1456-1462.
126. Leist M, Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms. Nat Rev Mol Cell Biol 2001; 2: 589-598.
127. Saraste A, Pulkki K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 2000; 45: 528-537.
128. Pellettieri J, Sánchez Alvarado A. Cell turnover and adult tissue homeostasis: from humans to planarians. Annu Rev Genet 2007; 41: 83-105.
129. Chera S, Ghila L, Dobretz K, et al. Apoptotic cells provide an unexpected source of Wnt3 signaling to drive hydra head regeneration. Dev Cell 2009; 17: 279-289.
130. Bergmann A, Steller H. Apoptosis, stem cells, and tissue regeneration. Sci Signal 2010; 3 re8.
131. Fan Y, Bergmann A. Apoptosis-induced compensatory proliferation. The cell is dead. Long live the cell! Trends Cell Biol 2008; 18: 467-473.
132. Tseng AS, Adams DS, Qiu D, Koustubhan P, Levin M. Apoptosis is required during early stages of tail regeneration in Xenopus laevis. Dev Biol 2007; 301: 62-69.
133. Domen J, Gandy KL, Weissman IL. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 1998; 91: 2272-2282.
134. Domen J, Weissman IL. Hematopoietic stem cells need two signals to prevent apoptosis BCL-2 can provide one of these, Kitl/c-Kit signaling the other. J Exp Med 2000; 192: 1707-1718.
135. Paus R, Rosenbach T, Haas N, Czarnetzki BM. Patterns of cell death: the significance of apoptosis for dermatology. Exp Dermatol 1993; 2: 3-11.
136. Polakowska RR, Piacentini M, Bartlett R, Goldsmith LA, Haake AR. Apoptosis in human skin development: morphogenesis, periderm, and stem cells. Dev Dyn 1994; 199: 176-188.
137. Sotiropoulou PA, Candi A, Mascré G, et al. Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death. Nat Cell Biol 2010; 12: 572-582.
138. 8+ lymphocytes and accumulation of Ki67 antigen. Bone Marrow Transplant 2000; 26: 1077-1082.
139. Hurwitz SA, Spandau DF. Quantitative analysis of UVB-induced apoptosis in human epidermis. Exp Dermatol 2000; 9: 185-191.
140. Haake AR, Roublevskaia I, Cooklis M. Apoptosis: a role in skin aging? J Investig Dermatol Symp Proc 1998; 3: 28-35.
141. Racila D, Bickenbach JR. Are epidermal stem cells unique with respect to aging? Aging 2009; 1: 746-750.
142. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 2002; 115: 2381-2388.
143. Aitken RJ, Findlay JK, Hutt KJ, Kerr JB. Apoptosis in the germ line. Reproduction 2011; 141: 139-150.
144. Zeuner A, Eramo A, Peschle C, De Maria R. Caspase activation without death. Cell Death Differ 1999; 6: 1075-10780.
145. Schwerk C, Schulze-Osthoff K. Non-apoptotic functions of caspases in cellular proliferation and differentiation. Biochem Pharmacol 2003; 66: 1453-1458.
146. Wang J, Walsh K. Resistance to apoptosis conferred by Cdk inhibitors during myocyte differentiation. Science 1996; 273: 359-361.
147. Dee K, Freer M, Mei Y, Weyman CM. Apoptosis coincident with the differentiation of skeletal myoblasts is delayed by caspase 3 inhibition and abrogated by MEK-independent constitutive Ras signaling. Cell Death Differ 2002; 9: 209-218.
148. Shaltouki A, Freer M, Mei Y, Weyman CM. Increased expression of the pro-apoptotic Bcl2 family member PUMA is required for mi-tochondrial release of cytochrome C and the apoptosis associated with skeletal myoblast differentiation. Apoptosis 2007; 12: 2143-2154.
149. Dominov JA, Dunn JJ, Miller JB. Bcl-2 expression identifies an early stage of myogenesis and promotes clonal expansion of muscle cells. J Cell Biol 1998; 142: 537-544.
150. Weedon D, Strutton G. Apoptosis as the mechanism of the involution of hair follicles in catagen transformation. Acta Derm Venereol 1981; 61: 335-339.
151. Messenger AG. The control of hair growth. J Invest Dermatol 1993; 101: 4-9.
152. Schneider MR, Schmidt-Ullrich R, Paus R. The hair follicle as a dynamic miniorgan. Curr Biol 2009; 19: 132-142.
153. Espada J, Varela I, Flores I, et al. Nuclear envelope defects cause stem cell dysfunction in premature-aging mice. J Cell Bio 2008; 181: 27-35.
154. Nishimura EK, Granter SR, Fisher DE. Mechanisms of hair graying: incomplete melanocyte stem cell maintenance in the niche. Science 2005; 307: 720-724.
155. Oguro H, Iwama A. Life and death in hematopoietic stem cells. Curr Opin Immunol 2007; 19: 503-509.
156. Chao DL, Eck JT, Brash DE, Maley CC, Luebeck EG. Preneoplas-tic lesion growth driven by the death of adjacent normal stem cells. Proc Natl Acad Sci USA 2008; 105: 1509-1534.
157. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100: 57-70.
158. Kruyt FA, Schuringa JJ. Apoptosis and cancer stem cells: implications for apoptosis targeted therapy. Biochem Pharmacol 2010; 80: 423-430.
159. Reguart N, He B, Taron M, You L, Jablons DM, Rosell R. The role of Wnt signaling in cancer and stem cells. Future Oncol 2005; 1: 787-797.
160. Wu XZ, Xie GR, Chen D. Hypoxia and hepatocellular carcinoma: the therapeutic target for hepatocellular carcinoma. J Gastroenterol Hepatol 2007; 22: 1178-1182.
161. Katoh M, Katoh M. WNT signaling pathway and stem cell signaling network. Clin Cancer Res 2007; 13: 4042-4045.
162. Chen QM, Liu J, Merrett JB. Apoptosis or senescence-like growth arrest: influence of cell-cycle position, p53, p21 and bax in H2O2 response of normal human fibroblasts. Biochem J 2000; 347: 543-551.
163. Hampel B, Malisan F, Niederegger H, Testi R, Jansen-Dürr P. Differential regulation of apoptotic cell death in senescent human cells. Exp Gerontol 2004; 39: 1713-1721.
164. Seluanov A, Gorbunova V, Falcovitz A, et al. Change of the death pathway in senescent human fibroblasts in response to DNA damage is caused by an inability to stabilize p53. Mol Cell Biol 2001; 21: 1552-1564.
165. Rebbaa A, Zheng X, Chou PM, Mirkin BL. Caspase inhibition switches doxorubicin-induced apoptosis to senescence. Oncogene 2003; 22: 2805-2811.
166. Blagosklonny MV, Darzynkiewicz Z. Strategies of protection of normal cells during chemo- and radio-therapy based on modulation of cell cycle and apoptotic pathways. In: Los M, Gibson SB, Eds. Apoptotic pathways as target for novel therapies in cancer and other diseases. New York, Springer Academic Press 2005; 357-391.
167. Wesselborg S, Lauber K. Mechanism of anticancer drug action. In: Los M, Gibson SB, Eds. Apoptotic pathways as target for novel therapies in cancer and other diseases. New York, Springer Academic Press 2005; 31-56.
168. Abdulghani J, El-Deiry WS. TRAIL receptor signaling and therapeutics. Expert Opin Ther Targets 2010; 14: 1091-1108.
169. Mellier G, Huang S, Shenoy K, Pervaiz S. TRAILing death in cancer. Mol Aspects Med 2010; 31: 93-112.
170. Roos WP, Kaina B. DNA damage-induced cell death by apoptosis. Trends Mol Med 2006; 12: 440-450.
171. Kelley SK, Ashkenazi A. Targeting death receptors in cancer with Apo2L/TRAIL. Curr Opin Pharmacol 2004; 4: 333-339.
172. Sprick MR, Walczak H. The interplay between the Bcl-2 family and death receptor-mediated apoptosis. Biochim Biophys Acta 2004; 1644: 125-132.
173. Siegel RM. Caspases at the crossroads of immune-cell life and death. Nat Rev Immunol 2006; 6: 308-317.
174. Philchenkov A, Zavelevich M, Kroczak TJ, Los M. Caspases and cancer: mechanisms of inactivation and new treatment modalities. Exp Oncol 2004; 26: 82-97.
175. Rowinsky EK. Targeted induction of apoptosis in cancer management: the emerging role of tumor necrosis factor-related apoptosis-inducing ligand receptor activating agents. J Clin Oncol 2005; 23: 9394-9407.
176. Salvesen GS, Abrams JM. Caspase activation-stepping on the gas or releasing the brakes? Lessons from humans and flies. Oncogene 2004; 23: 2774-2784.
177. Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407: 770-776.
178. Barczyk K, Kreuter M, Pryjma J, et al. Serum cytochrome c indicates in vivo apoptosis and can serve as a prognostic marker during cancer therapy. Int J Cancer 2005; 116: 167-173.
179. Kim JH, Kim HD, Ryu GH, Kim DH, Hurwitz J, Seo YS. Isolation of human DNA2 endonuclease and characterization of its enzymatic properties. Nucleic Acids Res 2006; 34: 1854-1864.
180. Halliwell B. Oxidative stress and cancer: have we moved forward? Biochem J 2007; 401: 1-11.
181. Blagosklonny MV. Aging: ROS or TOR. Cell Cycle 2008; 7: 3344-3354.
182. Yoon SO, Yun CH, Chung AS. Dose effect of oxidative stress on signal transduction in aging. Mech Ageing Dev 2002; 123: 1597-1604.
183. Maynard S, Schurman SH, Harboe C, de Souza-Pinto NC, Bohr VA. Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 2009; 30: 2-10.
184. Finkel T, Holbrook NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000; 408: 239-247.
185. Chandel NS, Budinger GR. The cellular basis for diverse response to oxygen. Free Rad Biol Med 2007; 42: 165-174.
186. Guo YL, Chakraborty S, Rajan SS, Wang R, Huang F. Effects of oxidative stress on mouse embryonic stem cell proliferation, apop-tosis, senescence, and self-renewal. Stem Cells Dev 2010; 19: 1321-1331.
187. Cao C, Lu S, Kivlin R, et al. AMP-activated protein kinase contributes to UV- and H2O2-induced apoptosis in human skin kerati-nocytes. J Biol Chem 2008; 283: 28897-28908.
188. Lu T, Finkel T. Free radicals and senescence. Exp Cell Res 2008; 314: 1918-1922.
189. Liu L, Trimarchi JR, Keefe DL. Involvement of mitochondria in oxidative stress-induced cell death in mouse zygotes. Biol Reprod 2000; 62: 1745-1753.
190. Leese HJ, Sturmey RG, Baumann CG, McEvoy TG. Embryo viability and metabolism: obeying the quiet rules. Hum Reprod 2007; 22: 3047-3050.
191. Harvey AJ, Kind KL, Thompson JG. REDOX regulation of early embryo development. Reproduction 2002; 123: 479-486.
192. Yang HW, Hwang KJ, Kwon HC, Kim HS, Choi KW, Oh KS. Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod 1998; 13: 998-1002.
193. Tilly JL. Commuting the death sentence: how oocytes strive to survive. Nat Rev Mol Cell Biol 2001; 2: 838-848.
194. Kim MR, Tilly JL. Current concepts in Bcl-2 family member regulation of female germ cell development and survival. Biochim Bio-phys Acta 2004; 1644: 205-210.
195. Tilly JL, Kowalski KIN, Johnson AL, Such AD. Involvement of apoptosis in ovarian follicles atresia and postovulatory regression. Endocrinology 1991; 129: 2799-2801.
196. Billig H, Furuta I, Hsueh AJ. Gonadotropin-releasing hormone directly induces apoptotic cell death in the rat ovary: biochemical and in situ detection of deoxyribonucleic acid fragmentation in granulosa cells. Endocrinology 1994; 134: 245-252.
197. Re RN, Cook JL. Senescence, apoptosis, and stem cell biology: the rationale for an expanded view of intracrine action. Am J Physiol Heart Circ Physiol 2009; 297: 893-901.
198. Salvesen GS, Dixit VM. Caspases: intracellular signaling by prote-olysis Cell 1997; 91: 443-446.
199. Thornberry NA, Rano TA, Peterson EP, et al. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J Biol Chem 1997; 272: 17907-17911.
200. Nicholson DW, Thornberry NA. Caspases: killer proteases. Trends Biochem Sci 1997; 22: 299-306.
201. Rao L, Perez D, White E. Lamin proteolysis facilitates nuclear events during apoptosis. J Cell Biol 1996; 135: 1441-1455.
202. Kothakota S, Azuma T, Reinhard C, et al. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 1997; 278: 294-298.
203. Tan X, Wang JY. The caspase-RB connection in cell death. Trends Cell Biol 1998; 8: 116-120.
204. Ramalho-Santos J, Varum S, Amaral S, Mota PC, Sousa AP, Amaral A. Mitochondrial functionality in reproduction: from go-nads and gametes to embryos and embryonic stem cells. Hum Re-prod Update 2009; 15: 553-572.
205. Hikim Sinha AP, Lue Y, Diaz-Romero M, Yen PH, Wang C, Swerdloff RS. Deciphering the pathways of germ cell apoptosis in the testis. J Steroid Biochem Mol Biol 2003; 85: 175-182.
206. Zheng S, Turner TT, Lysiak JJ. Caspase 2 activity contributes to the initial wave of germ cell apoptosis during the first round of spermatogenesis Biol Reprod 2006; 74: 1026-1033.
207. Li F, Huang Q, Chen J, et al. Apoptotic cells activate the phoenix rising pathway to promote wound healing and tissue regeneration. Sci Signal 2010; 3: ra13.
208. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell 2008; 132: 681-696.
209. Ganong BR. Roles of lipid turnover in transmembrane signal trans-duction. Am J Med Sci 1991; 302: 304-312.
210. Meyer S, Temme C, Wahle E. Messenger RNA turnover in eu-karyotes: pathways and enzymes. Crit Rev Biochem Mol Biol 2004; 39: 197-216.
211. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009; 137: 413-431.
212. Impicciatore G, Sancilio S, Miscia S, Di Pietro R. Nutlins and ionizing radiation in cancer therapy. Curr Pharm Des 2010; 16: 1427-1442.
213. Puzio-Kuter AM, Levine AJ. Stem cell biology meets p53. Nat Biotechnol 2009; 27: 914-915.
214. Zhao T, Xu Y. p53 and stem cells: new developments and new concerns. Trends Cell Biol 2010; 20: 170-175.
215. Vousden KH, Lu X. Live or let die: the cell's response to p53. Nat Rev Cancer 2002; 2: 594-604.
216. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006; 6: 909-923.
217. Avantaggiati ML, Ogryzko V, Gardner K, Giordano A, Levine AS, Kelly K. Recruitment of p300/CBP in p53-dependent signal pathways. Cell 1997; 89: 1175-1184.
218. Varley JM. Germline TP53 mutations and Li-Fraumeni syndrome. Hum Mutat 2003; 21: 313-320.
219. Wahl GM, Carr AM. The evolution of diverse biological responses to DNA damage: insights from yeast andp53. Nat Cell Biol 2001; 3: 277-286.
220. Yaswen P, Campisi J. Oncogene-induced senescence pathways weave an intricate tapestry. Cell 2007; 128: 295-308.
221. Hornsby PJ. Senescence as anticancer mechanism. J Clin Oncol 2007; 28: 177-186.
222. Roninson IB. Tumor cell senescence in cancer treatment. Cancer Res 2003; 63: 2705-2715.
223. Lehmann BD, McCubrey JA, Jefferson HS, Paine MS, Chappel WH, Terrian DM. A dominant role for p53 dependent cellular senescence in radiosensitization of human prostate cancer cells. Cell Cycle 2007; 6: 595-596.
224. Aladjem MI, Spike BT, Rodewald LW, et al. ES cells do not activate p53-dependent stress responses and undergo p53-independent apoptosis in response to DNA damage. Curr Biol 1998; 8: 145-155.
225. Chambers I, Smith A. Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 2004; 23: 7150-7160.
226. Chao C, Saito S, Anderson CW, Appella E, Xu Y. Phosphorylation of murine p53 at ser-18 regulates the p53 responses to DNA damage. Proc Natl Acad Sci USA 2000; 97: 11936-11941.
227. Bondar T, Medzhitov R. p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cells 2010; 6: 309-322.
228. Bonizzi G, Cicalese A, Insinga A, Pelicci PG. The emerging role of p53 in stem cells. Trends Mol Med 2011; 731: 1-7.
229. Feng Z, Lin M, Wu R. The regulation of aging and longevity: a new and complex role of p53. Genes Cancer 2011; 2: 443-452.
230. Gatza CE, Dumble M, Kittrell F, et al. Altered mammary gland development in the p53+/m mouse, a model of accelerated aging. Dev Biol 2008; 313: 130-141.
231. Dumble M, Moore L, Chambers SM, et al. The impact of altered p53 dosage on hematopoietic stem cell dynamics during aging. Blood 2007; 109: 1736-1742.
232. Donehower LA. Using mice to examine p53 functions in cancer, aging, and longevity. Cold Spring Harb Perspect Biol 2009; 1: 1-17.
233. García-Cao I, García-Cao M, Martín-Caballero J, et al. Super p53 mice exhibit enhanced DNA damage response, are tumor resistant and age normally. EMBO J 2002; 21: 6225-6235.
234. Mendrysa SM, O'Leary KA, McElwee MK, et al. Tumor suppression and normal aging in mice with constitutively high p53 activity. Genes Dev 2006; 20: 16-21.
235. TeKippe M, Harrison DE, Chen J. Expansion of hematopoietic stem cell phenotype and activity in Trp53-null mice. Exp Hematol 2003; 31: 521-527.
236. Akala OO, Park IK, Qian D, Pihalja M, Becker MW, Clarke MF. Long-term haematopoietic reconstitution by Trp53-/-p16Ink4a-/-p19Arf-/- multipotent progenitors. Nature 2008; 453: 228-232.
237. Zheng H, Ying H, Yan H, et al. Pten and p53 converge on c-Myc to control differentiation, self-renewal, and transformation of normal and neoplastic stem cells in glioblastoma. Cold Spring Harb Symp Quant Biol 2008; 73: 427-437.
238. Potten CS. Stem cells in gastrointestinal epithelium: numbers, characteristics and death. Philos Trans R Soc Lond B Biol Sci 1998; 353: 821-830.
239. D'Sa-Eipper C, Leonard JR, Putcha G, et al. DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3. Development 2001; 128: 137-146.
240. Schuler M, Green DR. Mechanisms of p53-dependent apoptosis. Biochem Soc Trans 2001; 29: 684-688.
241. Friedman JS, Lowe SW. Control of apoptosis by p53. Oncogene 2003; 22: 9030-9040.
242. Qin H, Yu T, Qing T, et al. Regulation of apoptosis and differentiation by p53 in human embryonic stem cells. J Biol Chem 2007; 282: 5842-5852.
243. Yu H, Shen H, Yuan Y, et al. Deletion of Puma protects hema-topoietic stem cells and confers long-term survival in response to high-dose gamma-irradiation. Blood 2010; 115: 3472-3480.
244. Asai T, Liu Y, Bae N, Nimer SD. The p53 tumor suppressor protein regulates hematopoietic stem cell fate. J Cell Physiol 2011; 226: 215-21.
245. Bongiovanni L, Müller EJ, Della Salda L. Survivin in skin pathologies. Exp Dermatol 2011; 20: 457-463.
246. Kastan MB, Radin AI, Kuerbitz SJ, et al. Levels of p53 protein increase with maturation in human hematopoietic cells. Cancer Res 1991; 51: 4279-4286.
247. Shounan Y, Dolnikov A, MacKenzie KL, Miller M, Chan YY, Symonds G. Retroviral transduction of hematopoietic progenitor cells with mutant p53 promotes survival and proliferation, modifies differentiation potential and inhibits apoptosis. Leukemia 1996; 10: 1619-28.
248. Sablina AA, Budanov AV, Ilyinskaya GV, Agapova LS, Kravchenko JE, Chumakov PM. The antioxidant function of the p53 tumor suppressor. Nat Med 2005; 11: 1306-1313.
249. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet 2006; 15: 17-29.
250. Hough SR, Clements I, Welch PJ, Wiederholt KA. Differentiation of mouse embryonic stem cells after RNA interference-mediated silencing of OCT4 and Nanog. Stem Cells 2006; 24: 1467-1475.
251. Sharov AA, Masui S, Sharova LV, et al. Identification of Pou5f1, Sox2, and Nanog downstream target genes with statistical confidence by applying a novel algorithm to time course microarray and genome-wide chromatin immunoprecipitation data. BMC Genom-ics 2008; 9: 269.
252. Liu N, Feng X, Fang Z, et al. Identification of genes regulated by nanog which is involved in ES cells pluripotency and early differentiation. J Cell Biochem 2008; 104: 2348-2362.
253. Tiscornia G, Izpisúa Belmonte JC. MicroRNAs in embryonic stem cell function and fate. Genes Dev 2010; 24: 2732-2741.
254. Wiemer EAC. The role of microRNAs in cancer: no small matter. Eur J Cancer 2007; 43: 1529-1544.
255. Glass C, Singla DK. ES cells overexpressing microRNA-1 attenuate apoptosis in the injured myocardium. Mol Cell Biochem 2011 Aug 26, Epub ahead of print.
256. Zernecke A, Bidzhekov K, Noels H, et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009; 2: ra81.
257. Siminovitch L, McCulloch EA, Till JE. The distribution of colony-forming cells among spleen colonies. J Cell Physiol 1963; 62: 327-336.
258. Bach FH, Albertini RJ, Joo P, Anderson JL, Bortin MM. Bone-marrow transplantation in a patient with the Wiskott-Aldrich syndrome. Lancet 1968; 2: 1364-1366.
259. Thomas ED, Flournoy N, Buckner CD, et al. Cure of leukemia by marrow transplantation. Leukemia Res 1977; 1: 67-70.
260. Korbling M, Dorken B, Ho AD, Pezzutto A, Hunstein W, Fliedner TM. Autologous transplantation of blood-derived hemopoietic stem cells after myeloablative therapy in a patient with Burkitt's lym-phoma. Blood 1986; 67: 529-532.
261. Ho AD, Punzel M. Hematopoietic stem cells: can old cells learn new tricks? J Leukoc Biol 2003; 73: 547-555.
262. Chen J. Senescence and functional failure in hematopoietic stem cells. Exp Hematol 2004; 32: 1025-1032.
263. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA 1992; 89: 2804-2808.
264. Craig W, Kay R, Cutler RL, Lansdorp PM. Expression of Thy-1 on human hematopoietic progenitor cells. J Exp Med 1993; 177: 1331-1342.
265. Attar EC, Scadden DT. Regulation of hematopoietic stem cell growth. Leukemia 2004; 18: 1760-1768.
266. Eaves AC, Eaves CJ. Erythropoiesis in culture. Clin Haematol 1984; 13: 371-391.
267. Hoffman R. Regulation of megakaryocytopoiesis. Blood. 1989;74:1196.
268. Metcalf D. Control of granulocytes and macrophages: molecular, cellular, and clinical aspects. Science 1991; 254:529-533.
269. Ogawa M. Differentiation and proliferation of hematopoietic stem cells. Blood 1993; 81: 2844-2853.
270. Novak JP, Stewart CC. Stochastic versus deterministic in haemopoiesis: what is what? Br J Haematol 1991; 78: 149-154.
271. McCormick A, Campisi J. Cellular aging and senescence. Curr Opin Cell Biol 1991; 3: 230-234.
272. Krishnamurthy J, Torrice C, Ramsey MR, et al. Ink4a/Arf expression is a biomarker of aging. J Clin Invest 2004; 114: 1299-1307.
273. Janzen V, Forkert R, Fleming HE, et al. Stem-cell ageing modified by the cyclin-dependent kinase inhibitor p16INK4a. Nature 2006; 443: 421-426.
274. Lotem J, Sachs L. Hematopoietic cells from mice deficient in wild-type p53 are more resistant to induction of apoptosis by some agents. Blood 1993; 82: 1092-1096.
275. Tyner SD, Venkatachalam S, Choi J, et al. p53 mutant mice that display early ageing-associated phenotypes. Nature 2002; 415: 45-53.
276. Maier B, Gluba W, Bernier B, et al. Modulation of mammalian life span by the short isoform of p53. Genes Dev 2004; 18: 306-319.
277. Garcia-Cao I, Garcia-Cao M, Tomas-Loba A, et al. Increased p53 activity does not accelerate telomere-driven ageing. EMBO Rep 2006; 7: 546-552.
278. Di Pietro R, Secchiero P, Rana R, et al. Ionizing radiation sensitizes erythroleukemic cells but not normal erythroblasts to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-mediated cytotoxicity by selective up-regulation of TRAIL-R1. Blood 2001; 97: 2596-2603.
279. Migliaccio G, Di Pietro R, Di Giacomo V, et al. In vitro mass production of human erythroid cells from the blood of normal donors and of thalassemic patients. Blood Cells Mol Dis 2002; 28: 169-180.
280. Campioni D, Secchiero P, Corallini F, et al. Evidence for a role of TNF-related apoptosis-inducing ligand (TRAIL) in the anemia of myelodysplastic syndromes. Am J Pathol 2005; 166: 557-563.
281. Secchiero P, Zauli G. Tumor necrosis factor-related apoptosis-inducing ligand and the regulation of hematopoiesis. Curr Opin Hematol 2008; 15: 42-48.
282. Zamai L, Secchiero P, Pierpaoli S, et al. TNF-related apoptosis-inducingligand (TRAIL) as a negative regulator of normal human erythropoiesis. Blood 2000; 95: 3716-3724.
283. De Maria R, Zeuner A, Eramo A, et al. Negative regulation of erythropoiesis by caspase-mediated cleavage of GATA-1. Nature 1999; 401: 489-493.
284. Secchiero P, Melloni E, Heikinheimo M, et al. TRAIL regulates normal erythroid maturation through an ERK-dependent pathway. Blood 2004; 103: 517-522.
285. Mirandola P, Gobbi G, Ponti C, Sponzilli I, Cocco L, Vitale M. PKCepsilon controls protection against TRAIL in erythroid progenitors. Blood 2006; 107: 508-513.
286. Alenzi FQ. Links between apoptosis, cell cycle and proliferation. Br J Biomed Sci 2004; 61: 99-102.
287. Alenzi FQ, Tamimi W, Al-Sebiany A, et al. Apoptosis role of Fas/Fas Ligand System in the Regulation of Myelopoesis. YJBM 2005; 78: 25-36.
288. Tothova Z, Kollipara R, Huntly BJ, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128: 325-339.
289. Cheng T, Rodrigues N, Shen H, et al. Hematopoietic stem cell quiescence maintained by p21cip1/waf1. Science 2000; 287: 1804-1808.
290. Mauro A. Satellite cells of skeletal muscle fibers. J Biophys Bio-chem Cytol 1961; 9: 493-495.
291. th ed. New York, Mc Graw-Hill 1994; 1: 97-118.
292. Asakura A. Stem cells in adult skeletal muscle. Trends Cardiovasc Med 2003; 13: 123-128.
293. Jankowski RJ, Deasy BM, Huard J. Muscle-derived stem cells. Gene Ther 2002; 9: 642-647.
294. Burdzihska A, Gala K, Paczek L. Myogenic stem cells. Folia His-tochem Cytobiol 2008; 46: 401-412.
295. Cooper RN, Butler-Browne GS, Mouly V. Human muscle stem cells. Curr Opin Pharmacol 2006; 6: 295-300.
296. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA. Pax7 is required for the specification of myogenic satellite cells. Cell 2000; 102: 777-786.
297. Yablonka-Reuveni Z, Day K, Vine A, Shefer G. Defining the transcriptional signature of skeletal muscle stem cells. J Anim Sci 2008; 86: 207-16.
298. Ludolph DC, Konieczny SF. Transcription factor families: muscling in on the myogenic program. FASEB J 1995; 9: 1595-1604.
299. Rudnicki MA, Le Grand F, McKinnell I, Kuang S. The molecular regulation of muscle stem cell function. Cold Spring Harb Symp Quant Biol 2008; 73: 323-331.
300. Yablonka-Reuveni Z, Rivera AJ. Temporal expression of regulatory and structural muscle proteins during myogenesis of satellite cells on isolated adult rat fibers. Dev Biol 1994; 164: 588-603.
301. Zammit PS, Partridge TA, Yablonka-Reuveni Z. The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histo-chem Cytochem 2006; 54: 1177-1191.
302. Molkentin JD, Olson EN. Combinatorial control of muscle development by basic helix-loop-helix and MADS box transcription factors. Proc Natl Acad Sci USA 1996; 93: 9366-9373.
303. Gianakopoulos PJ, Mehta V, Voronova A, et al. MyoD directly up-regulates premyogenic mesoderm factors during induction of skeletal myogenesis in stem cells. J Biol Chem 2011; 286: 2517-2525.
304. Zammit PS. All muscle satellite cells are equal, but are some more equal than others? J Cell Sci 2008; 121: 2975-2982.
305. Kuang S, Kuroda K, Le Grand F, Rudnicki MA. Asymmetric self-renewal and commitment of satellite stem cells in muscle. Cell 2007; 129: 999-1010.
306. Brack A, Conboy IM, Conboy MJ, Shen J, Rando TA. A temporal switch from Notch to Wnt signaling in muscle stem cells is necessary for normal adult myogenesis. Cell Stem Cell 2008; 2: 50-59.
307. Abou-Khalil R, le Grand F, Pallafacchina G, et al. Autocrine and paracrine angiopoietin 1/Tie-2 signaling promotes muscle satellite cell self-renewal. Cell Stem Cell 2009; 4: 298-309.
308. Kang JS, Krauss RS. Muscle stem cells in developmental and regenerative myogenesis. Curr Opin Clin Nutr Metab Care 2010; 13: 243-248.
309. Kuang S, Gillespie MA, Rudnicki MA. Niche regulation of muscle satellite cell self-renewal and differentiation. Cell Stem Cell 2008; 2: 22-31.
310. Scadden DT. The stem-cell niche as an entity of action. Nature 2006; 441: 1075-1079.
311. Gopinath SD, Rando TA. Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell 2008; 7: 590-598.
312. Roth SM, Martel GF, Ivey FM, et al. Skeletal muscle satellite cell populations in healthy young and older men and women. Anat Rec 2000; 260: 351-358.
313. Beccafico S, Puglielli C, Pietrangelo T, Bellomo R, Fanò G, Fulle S. Age-dependent effects on functional aspects in human satellite cells. Ann N Y Acad Sci 2007; 1100: 345-352.
314. Fulle S, Di Donna S, Puglielli C, et al. Age-dependent imbalance of the antioxidative system in human satellite cells. Exp Gerontol 2005; 40: 189-197.
315. Thornell LE, Lindström M, Renault V, Mouly V, Butler-Browne GS. Satellite cells and training in the elderly. Scand J Med Sci Sports 2003; 13: 48-55.
316. Jejurikar SS, Kuzon WM. Satellite cell depletion in degenerative skeletal muscle. Apoptosis 2003; 8: 573-578.
317. Beccafico S, Riuzzi F, Puglielli C, et al. Human muscle satellite cells show age-related differential expression of S100B protein and RAGE. Age 2011; 33: 523-541.
318. Collins M, Renault V, Grobler LA, St Clair Gibson A, Lambert MI, Wayne Derman E, et al. Athletes with exercise-associated fatigue have abnormally short muscle DNA telomeres. Med Sci Sports Ex-erc 2003; 35: 1524-1528.
319. Ponsot E, Lexell J, Kadi F. Skeletal muscle telomere length is not impaired in healthy physically active old women and men. Muscle Nerve 2008; 37: 467-472.
320. Kadi F, Ponsot E, Piehl-Aulin K, et al. The effects of regular strength training on telomere length in human skeletal muscle. Med Sci Sports Exerc 2008; 40: 82-87.
321. Di Donna S, Renault V, Forestier C, et al. Regenerative capacity of human satellite cells: the mitotic clock in cell transplantation. Neu-rol Sci 2000; 21: 943-951.
322. Kadi F, Charifi N, Denis C, Lexell J. Satellite cells and myonuclei in young and elderly women and men. Muscle Nerve 2004: 29; 120-127.
323. Peterson CA. Cell culture systems as tools for studying age-related changes in skeletal muscle. J Gerontol A Biol Sci Med Sci 1995; 50: 142-144.
324. Taylor-Jones JM, McGehee RE, Rando TA, Lecka-Czernik B, Lipschitz DA, Peterson CA. Activation of an adipogenic program in adult myoblasts with age. Mech Ageing Dev 2002; 123: 649-661.
325. Jejurikar SS, Henkelman EA, Cederna PS, Marcelo CL, Urbanchek MG, Kuzon WM. Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis. Exp Gerontol 2006; 41: 828-836.
326. Sancilio S, Puglielli C, Caprara M, Fulle S, Di Pietro R. Age-related effects on apoptosis of human satellite cells. Eur J Histo-chem 2009; 53:33.
327. Fernando P, Kelly JF, Balazsi K, Slack RS, Megeney LA. Caspase 3 activity is required for skeletal muscle differentiation. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:11025.
328. Hunt LC, Upadhyay A, Jazayeri JA, Tudor EM, White JD. Caspase-3, myogenic transcription factors and cell cycle inhibitors are regulated by leukemia inhibitory factor to mediate inhibition of myogenic differentiation. Skelet Muscle 2011; 1: 1-13.
329. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 2003; 162: 1135-1147.
330. Siriett V, Platt L, Salerno MS, Ling N, Kambadur R, Sharma M. Prolonged absence of myostatin reduces sarcopenia. J Cell Physiol 2006; 209: 866-873.
331. McFarlane C, Hui GZ, Amanda WZ, et al. Human myostatin negatively regulates human myoblast growth and differentiation. Am J Physiol Cell Physiol 2011; 301: 195-203.
332. Manceau M, Gros J, Savage K, et al. Myostatin promotes the terminal differentiation of embryonic muscle progenitors. Genes Dev 2008; 22: 668-681.
333. Chew SL, Lavender P, Clark AJ, Ross RJ. An alternatively spliced human insulin-like growth factor-I transcript with hepatic tissue expression that diverts away from the mitogenic IBE1 peptide. Endocrinology 1995; 136: 1939-1944.
334. Daughaday WH, Rotwein P. Insulin-like growth factors I and II peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr Rev 1989; 10: 68-91.
335. Hameed M, Orrell RW, Cobbold M, Goldspink G, Harridge SD. Expression of IGF-I splice variants in young and old human skeletal muscle after high resistance exercise. J Physiol 2003; 547: 247-254.
336. Yang SY, Goldspink G. Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 2002; 522: 156-160.
337. Mills P, Lafreniere JF, Benabdallah BF, El Fahime el M, Tremblay JP. A new pro-migratory activity on human myogenic precursor cells for a synthetic peptide within the E domain of the mechano growth factor. Exp Cell Res 2007; 313: 527-537.
338. Goldspink G, Harridge SD. Growth factors and muscle ageing. Exp Gerontol 2004; 39: 1433-1438.
339. Goldspink G. Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 1999; 194: 323-334.
340. Musarò A, McCullagh K, Paul A, Houghton L, Dobrowolny G, Molinaro M, et al. Localized IGF-1 transgene expression sustains hypertrophy and regeneration in senescent skeletal muscle. Nat Genet 2001; 27: 195-200.
341. Campion DR. The muscle satellite cell: a review. Int Rev Cytol 1984; 87: 225-251.
342. Yang H, Alnaqeeb M, Simpson H, Goldspink G. Changes in muscle fibre type, muscle mass and IGF-I gene expression in rabbit skeletal muscle subjected to stretch. J Anat 1997; 190: 613-622.
343. Owino V, Yang SY, Goldspink G. Age-related loss of skeletal muscle function and the inability to express the autocrine form of insulin-like growth factor-1 (MGF) in response to mechanical overload. FEBS Lett 2001; 505: 259-263.
344. Renault V, Thornell LE, Eriksson PO, Butler-Browne G, Mouly V. Regenerative potential of human skeletal muscle during aging. Aging Cell 2002; 1: 132-139.
345. Kandalla PK, Goldspink G, Butler-Browne G, Mouly V. Mechano Growth Factor E peptide (MGF-E), derived from an isoform of IGF-1, activates human muscle progenitor cells and induces an increase in their fusion potential at different ages. Mech Ageing Dev 2011; 132: 154-162.
346. Barton ER. Viral expression of insulin-like growth factor-I iso-forms promotes different responses in skeletal muscle. J Appl Physiol 2006; 100: 1778-1784.
347. Pietrangelo T, Puglielli C, Mancinelli R, Beccafico S, Fanò G, Fulle S. Molecular basis of the myogenic profile of aged human skeletal muscle satellite cells during differentiation. Exp Gerontol 2009; 44: 523-531.
348. Brack AS, Conboy MJ, Roy S, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007; 317: 807-810.
349. Mecocci P, Fanò G, Fulle S, et al. Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Rad Biol Med 1999; 26: 303-308.
350. Fanò G, Mecocci P, Vecchiet J, Belia S, Fulle S, Polidori MC, et al. Age and sex influence on oxidative damage and functional status in human skeletal muscle. J Muscle Res Cell Motil 2001; 22: 345-351.
351. Renault V, Piron-Hamelin G, Forestier C, et al. Skeletal muscle regeneration and the mitotic clock. Exp Gerontol 2000; 35: 711-719.
352. Terman A, Brunk UT. On the degradability and exocytosis of ceroid/lipofuscin in cultured rat cardiac myocytes. Mech Age Dev 1998; 100: 145-156.
353. Renault V, Roland E, Thornell LE, Moule V, Butler-Browne G. Distribution of satellite cells in the human vastus lateralis muscle during aging. Exp Gerontol 2002; 37: 1513-1514.
354. Squier TC, Bigelow DJ. Protein oxidation and age-dependent alterations in calcium homeostasis. Front Biosci 2000; 5: 504-526.
355. Fulle S, Protasi F, Di Tano G, et al. The contribution of reactive oxygen species to sarcopenia and muscle ageing. Exp Gerontol 2004; 39: 17-24.
356. Jackson MJ, Papa S, Bolaños J, et al. Antioxidants, reactive oxygen and nitrogen species, gene induction and mitochondrial function. Mol Aspects Med 2002; 23: 209-285.
357. Arbogast S, Reid MB. Oxidant activity in skeletal muscle fibers is influenced by temperature, CO2 level, and muscle-derived nitric oxide. Am J Physiol 2004; 287: 698-705.
358. Silveira LR, Pereira LS, Juel C, Hellsten Y. Formation of hydrogen peroxide and nitric oxide in rat skeletal muscle cells during contractions. Free Radic Biol Med 2003; 35: 455-464.
359. Pattwell DM, McArdle A, Morgan JE, Patridge TA, Jackson MJ. Release of reactive oxygen and nitrogen species from contracting skeletal muscle cells. Free Radic Biol Med 2004; 37: 1064-1072.
360. Janssen MW, Houten BV, Borm PJA, Mossman BT. Biology of disease, cell and tissue response to oxidative damage. Lab Invest 1993; 69: 261-274.
361. Sen CK, Packer L. Antioxidant and redox regulation of gene transcription. FASEB J 1996; 10: 709-720.
362. Alvarez R, Vázquez P, Pérez F, et al. Regulation of fast skeletal muscle activity by SERCA1 vicinal-cysteines. J Muscle Res Cell Motil 2009; 30: 5-16.
363. Martindale JL, Holbrook NJ. Cellular response to oxidative stress: signal for suicide and survival. J Cell Physiol 2002; 192: 1-15.
364. Simon P, Fehrenbach E, Niess AM. Regulation of immediate early gene expression by exercise: short-cuts for the adaptation of immune function. Exerc Immunol Rev 2006; 12: 112-131.
365. Calabrese EJ, Baldwin LA. Hormesis at the National Toxicology Program (NTP): evidence of hormetic dose responses in NTP dose-range studies. Nonlinearity Biol Toxicol Med 2003; 1: 455-467.
366. Musarò A, Fulle S, Fanò G. Oxidative stress and muscle homeosta-sis. Curr Opin Clin Nutr Metab Care 2010; 13: 236-242.
367. McComas AJ, Sica RE. Automatic quantitative analysis of the electromyogram in partially denervated distal muscles: comparison with motor unit counting. Can J Neurol Sci 1978; 5: 377-383.
368. Lexell J, Taylor CC, Sjöström M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 1988; 84: 275-294.
369. Alway SE, Siu PM. Nuclear apoptosis contributes to sarcopenia. Exerc Sport Sci Rev 2008; 36: 51-57.
370. Brack AS, Bildsoe H, Hughes SM. Evidence that satellite cell decrement contributes to preferential decline in nuclear number from large fibres during murine age-related muscle atrophy. J Cell Sci 2005; 118: 4813-4821.
371. Rantanen T, Guralnik JM, Foley D, et al. Midlife hand grip strength as a predictor of old age disability. JAMA 1999; 281: 558-560.
372. Sandri M, Sandri C, Gilbert A, et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117: 399-412.
373. Bois PR, Grosveld GC. FKHR (FOXO1a) is required for myotube fusion of primary mouse myoblasts. EMBO J 2003; 22: 1147-1157.
374. Dupont-Versteegden EE, Strotman BA, Gurley CM, et al. Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei. Am J Physiol Regul Integr Comp Physiol 2006; 291: 1730-1740.
375. Tonkonogi M, Fernström M, Walsh B, et al. Reduced oxidative power but unchanged antioxidative capacity in skeletal muscle from aged humans. Pflugers Arch 2003; 446: 261-269.
376. Prigol M, Luchese C, Nogueira CW. Antioxidant effect of diphenyl diselenide on oxidative stress caused by acute physical exercise in skeletal muscle and lungs of mice. Cell Biochem Funct 2009; 27: 216-222.
377. Fisher-Wellman K, Bloomer RJ. Acute exercise and oxidative stress: a 30 year history. Dyn Med 2009; 8: 1-25.
378. Sinha S, Ray US, Saha M, Singh SN, Tomar OS. Antioxidant and redox status after maximal aerobic exercise at high altitude in acclimatized lowlanders and native highlanders. Eur J Appl Physiol 2009; 106: 807-814.
379. Sinha S, Singh SN, Saha M, Kain TC, Tyagi AK, Ray US. Antioxidant and oxidative stress responses of sojourners at high altitude in different climatic temperatures. Int J Biometeorol 2010; 54: 85-92.
380. Fulle S, Fanò G. The contribution of reactive oxygen species in sarcopenia and muscle aging. In: Stocchi V Ed. Role of physical exercise in disease prevention and quality of life improvement. SECTION III Physical Exercise and Oxidative Stress. Milano, Springer Verlag 2007; 103-111.