Heterochronic parabiosis for the study of the effects of aging on stem cells and their niches

Cell Cycle

Volumn 11, Issue 12, 2012, Pages 2260-2267

  Conboy, Irina M ^a,b   Rando, Thomas A ^c,d  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d VA PALO ALTO HEALTH CARE SYSTEM   (United States)

Author keywords

Aging; Muscle; Niche; Parabiosis; Stem cells

Indexed keywords

EOTAXIN; GENOMIC DNA; TRANSCRIPTION FACTOR C MAF; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; WNT PROTEIN;

AGE DISTRIBUTION; AGING; BIOCHEMISTRY; CELL AGING; CELL FUNCTION; DNA STRAND; HEMATOPOIETIC STEM CELL; HETEROCHRONIC PARABIOSIS; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; MORPHOGENESIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; OSTEOLYSIS; OSTEOPOROSIS; PARABIOSIS; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; STEM CELL; TELOMERE HOMEOSTASIS; TISSUE REGENERATION; TISSUE REPAIR;

MAMMALIA; METAZOA; MUS;

EID: 84862860608     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.20437     Document Type: Review

References (62)

1. Harrison DE. Long-term erythropoietic repopulating ability of old, young and fetal stem cells. J Exp Med 1983; 157:1496-504; PMID:6854204; http://dx.doi.org/10.1084/jem.157.5.1496.
2. Carlson BM, Faulkner JA. Muscle transplantation between young and old rats: age of host determines recovery. Am J Physiol 1989; 256:1262-6;PMID: 2735398.
3. 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; 433:760-4; PMID:15716955; http://dx.doi.org/10.1038/ nature03260.
4. Brack AS, Conboy MJ, Roy S, Lee M, Kuo CJ, Keller C, et al. Increased Wnt signaling during aging alters muscle stem cell fate and increases fibrosis. Science 2007; 317:807-10; PMID:17690295; http://dx.doi.org/10.1126/science. 1144090.
5. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, et al. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 2011; 477:90-4; PMID:21886162; http://dx.doi.org/10.1038/nature10357.
6. Conboy IM, Yousef H, Conboy MJ. Embryonic antiaging niche. Aging (Albany NY) 2011; 3:555-63; PMID:21666284.
7. Conboy IM, Rando TA. Aging, stem cells and tissue regeneration: lessons from muscle. Cell Cycle 2005; 4:407-10; PMID:15725724; http://dx.doi.org/10. 4161/cc.4.3.1518.
8. Conboy IM, Conboy MJ, Smythe GM, Rando TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003; 302:1575-7; PMID:14645852; http://dx.doi.org/10.1126/science.1087573.
9. Carlson ME, Hsu M, Conboy IM. Imbalance between pSmad3 and Notch induces CDK inhibitors in old muscle stem cells. Nature 2008; 454:528- 32; PMID:18552838; http://dx.doi.org/10.1038/nature07034.
10. Carlson ME, Conboy MJ, Hsu M, Barchas L, Jeong J, Agrawal A, et al. Relative roles of TGF-beta1 and Wnt in the systemic regulation and aging of satellite cell responses. Aging Cell 2009; 8:676-89; PMID:19732043; http://dx.doi.org/10.1111/j.1474-9726.2009.00517.x.
11. Liu L, Rando TA. Manifestations and mechanisms of stem cell aging. J Cell Biol 2011; 193:257- 66; PMID:21502357; http://dx.doi.org/10.1083/jcb.201010131.
12. Sahin E, Depinho RA. Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 2010; 464:520-8; PMID:20336134; http://dx.doi.org/10.1038/nature08982.
13. Rando TA. Stem cells, ageing and the quest for immortality. Nature 2006; 441:1080-6; PMID:16810243; http://dx.doi.org/10.1038/nature04958.
14. He S, Nakada D, Morrison SJ. Mechanisms of stem cell self-renewal. Annu Rev Cell Dev Biol 2009; 25:377-406; PMID:19575646; http://dx.doi. org/10.1146/annurev.cellbio.042308.113248.
15. Knoblich JA. Mechanisms of asymmetric stem cell division. Cell 2008; 132:583-97; PMID:18295577; http://dx.doi.org/10.1016/j.cell.2008.02.007.
16. Rujano MA, Bosveld F, Salomons FA, Dijk F, van Waarde MA, van der Want JJ, et al. Polarised asymmetric inheritance of accumulated protein damage in higher eukaryotes. PLoS Biol 2006; 4:417; PMID:17147470; http://dx.doi.org/10. 1371/journal.pbio.0040417.
17. Yamashita YM, Mahowald AP, Perlin JR, Fuller MT. Asymmetric inheritance of mother versus daughter centrosome in stem cell division. Science 2007; 315:518-21; PMID:17255513; http://dx.doi.org/10.1126/science.1134910.
18. Cairns J. Mutation selection and the natural history of cancer. Nature 1975; 255:197-200; PMID:1143315; http://dx.doi.org/10.1038/255197a0.
19. Lark KG, Consigli RA, Minocha HC. Segregation of sister chromatids in mammalian cells. Science 1966; 154:1202-5; PMID:5921385; http://dx.doi.org/10. 1126/science.154.3753.1202.
20. Lark KG. Regulation of chromosome replication and segregation in bacteria. Bacteriol Rev 1966; 30:3-32; PMID:5324649.
21. Lark KG. Nonrandom segregation of sister chromatids in Vicia faba and Triticum boeoticum. Proc Natl Acad Sci USA 1967; 58:352-9; PMID:5231616; http://dx.doi.org/10.1073/pnas.58.1.352.
22. Potten CS, Hume WJ, Reid P, Cairns J. The segregation of DNA in epithelial stem cells. Cell 1978; 15:899-906; PMID:728994; http://dx.doi.org/10. 1016/0092-8674(78)90274-X.
23. Potten CS, Owen G, Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J Cell Sci 2002; 115:2381-8; PMID:12006622.
24. Conboy MJ, Karasov AO, Rando TA. High incidence of non-random template strand segregation and asymmetric fate determination in dividing stem cells and their progeny. PLoS Biol 2007; 5:102; PMID:17439301; http://dx.doi.org/10.1371/ journal.pbio.0050102.
25. Shinin V, Gayraud-Morel B, Gomès D, Tajbakhsh S. Asymmetric division and cosegregation of template DNA strands in adult muscle satellite cells. Nat Cell Biol 2006; 8:677-87; PMID:16799552; http://dx.doi.org/10.1038/ ncb1425.
26. Karpowicz P, Morshead C, Kam A, Jervis E, Ramunas J, Cheng V, et al. Support for the immortal strand hypothesis: neural stem cells partition DNA asymmetrically in vitro. J Cell Biol 2005; 170:721- 32; PMID:16115957; http://dx.doi.org/10.1083/jcb.200502073.
27. Smith GH. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 2005; 132:681-7; PMID:15647322; http://dx.doi.org/10.1242/dev.01609.
28. Karpowicz P, Pellikka M, Chea E, Godt D, Tepass U, van der Kooy D. The germline stem cells of Drosophila melanogaster partition DNA non-randomly. Eur J Cell Biol 2009; 88:397-408; PMID:19395121; http://dx.doi.org/10.1016/j.ejcb. 2009.03.001.
29. Schultz E, Gibson MC, Champion T. Satellite cells are mitotically quiescent in mature mouse muscle: an EM and radioautographic study. J Exp Zool 1978; 206:451-6; PMID:712350; http://dx.doi.org/10.1002/jez.1402060314.
30. Conboy IM, Rando TA. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev Cell 2002; 3:397-409; PMID:12361602; http://dx.doi.org/10.1016/S1534-5807(02)00254-X.
31. Gnocchi VF, White RB, Ono Y, Ellis JA, Zammit PS. Further characterisation of the molecular signature of quiescent and activated mouse muscle satellite cells. PLoS One 2009; 4:5205; PMID:19370151; http:// dx.doi.org/10.1371/journal.pone.0005205.
32. Pisconti A, Cornelison DD, Olguín HC, Antwine TL, Olwin BB. Syndecan-3 and Notch cooperate in regulating adult myogenesis. J Cell Biol 2010; 190:427-41; PMID:20696709; http://dx.doi.org/10.1083/jcb.201003081.
33. Acharyya S, Sharma SM, Cheng AS, Ladner KJ, He W, Kline W, et al. TNF inhibits Notch-1 in skeletal muscle cells by Ezh2 and DNA methylation mediated repression: implications in duchenne muscular dystrophy. PLoS One 2010; 5:12479; PMID:20814569; http://dx.doi.org/10.1371/journal.pone.0012479.
34. Brack AS, Murphy-Seiler F, Hanifi J, Deka J, Eyckerman S, Keller C, et al. BCL9 is an essential component of canonical Wnt signaling that mediates the differentiation of myogenic progenitors during muscle regeneration. Dev Biol 2009; 335:93- 105; PMID:19699733; http://dx.doi.org/10.1016/j. ydbio.2009.08.014.
35. Brack AS, 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; 2:50-9; PMID:18371421; http://dx.doi.org/10. 1016/j.stem.2007.10.006.
36. Scimè A, Desrosiers J, Trensz F, Palidwor GA, Caron AZ, Andrade-Navarro MA, et al. Transcriptional profiling of skeletal muscle reveals factors that are necessary to maintain satellite cell integrity during ageing. Mech Ageing Dev 2010; 131:9-20; PMID:19913570; http://dx.doi.org/10.1016/j.mad. 2009.11.001.
37. Carlson ME, Conboy IM. Regulating the Notch pathway in embryonic, adult and old stem cells. Curr Opin Pharmacol 2007; 7:303-9; PMID:17475556; http://dx.doi.org/10.1016/j.coph.2007.02.004.
38. Kuhn HG, Dickinson-Anson H, Gage FH. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 1996; 16:2027-33; PMID:8604047.
39. Maslov AY, Barone TA, Plunkett RJ, Pruitt SC. Neural stem cell detection, characterization and age-related changes in the subventricular zone of mice. J Neurosci 2004; 24:1726-33; PMID:14973255; http://dx.doi. org/10.1523/JNEUROSCI. 4608-03.2004.
40. Kempermann G, Brandon EP, Gage FH. Environmental stimulation of 129/SvJ mice causes increased cell proliferation and neurogenesis in the adult dentate gyrus. Curr Biol 1998; 8:939-42; PMID:9707406; http://dx.doi.org/10.1016/S0960- 9822(07)00377-6.
41. van Praag H, Kempermann G, Gage FH. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2:266-70; PMID:10195220; http://dx.doi.org/10.1038/6368.
42. Cameron HA, McKay RD. Restoring production of hippocampal neurons in old age. Nat Neurosci 1999; 2:894-7; PMID:10491610; http://dx.doi.org/10.1038/13197.
43. Montaron MF, Drapeau E, Dupret D, Kitchener P, Aurousseau C, Le Moal M, et al. Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol Aging 2006; 27:645-54; PMID:15953661; http://dx.doi.org/10.1016/j.neurobiolaging.2005.02.014.
44. Ergen AV, Goodell MA. Mechanisms of hematopoietic stem cell aging. Exp Gerontol 2010; 45:286- 90; PMID:20034552; http://dx.doi.org/10.1016/j.exger. 2009.12.010.
45. Chen C, Liu Y, Liu Y, Zheng P. mTOR regulation and therapeutic rejuvenation of aging hematopoietic stem cells. Sci Signal 2009; 2:75; PMID:19934433; http://dx.doi.org/10.1126/scisignal.2000559.
46. Konuma T, Oguro H, Iwama A. Role of the polycomb group proteins in hematopoietic stem cells. Dev Growth Differ 2010; 52:505-16; PMID:20646023; http://dx.doi.org/10.1111/j.1440-169X.2010.01191.x.
47. Wagner W, Horn P, Bork S, Ho AD. Aging of hematopoietic stem cells is regulated by the stem cell niche. Exp Gerontol 2008; 43:974-80; PMID:18504082; http://dx.doi.org/10.1016/j.exger.2008.04.007.
48. Takubo K, Goda N, Yamada W, Iriuchishima H, Ikeda E, Kubota Y, et al. Regulation of the HIF- 1alpha level is essential for hematopoietic stem cells. Cell Stem Cell 2010; 7:391-402; PMID:20804974; http://dx.doi.org/10.1016/j.stem. 2010.06.020.
49. Stenderup K, Justesen J, Clausen C, Kassem M. Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells. Bone 2003; 33:919-26; PMID:14678851; http://dx.doi.org/10.1016/j.bone. 2003.07.005.
50. Lu C, Miclau T, Hu D, Hansen E, Tsui K, Puttlitz C, et al. Cellular basis for age-related changes in fracture repair. J Orthop Res 2005; 23:1300-7; PMID:15936915.
51. Nishikawa K, Nakashima T, Takeda S, Isogai M, Hamada M, Kimura A, et al. Maf promotes osteoblast differentiation in mice by mediating the agerelated switch in mesenchymal cell differentiation. J Clin Invest 2010; 120:3455-65; PMID:20877012; http://dx.doi.org/10.1172/JCI42528.
52. Sun Y, Li W, Lu Z, Chen R, Ling J, Ran Q, et al. Rescuing replication and osteogenesis of aged mesenchymal stem cells by exposure to a young extracellular matrix. FASEB J 2011; 25:1474-85; PMID:21248241; http://dx.doi.org/10.1096/fj.10-161497.
53. Lo Celso C, Fleming HE, Wu JW, Zhao CX, Miake- Lye S, Fujisaki J, et al. Live-animal tracking of individual haematopoietic stem/progenitor cells in their niche. Nature 2009; 457:92-6; PMID:19052546; http://dx.doi.org/10.1038/ nature07434.
54. Hida D, Ishiguro N, Haneda M, Ishida Y, Suzuki H, Isobe K. Intra-bone marrow bone marrow transplantation rejuvenates the B-cell lineage in aged mice. Immunol Cell Biol 2010; 88:87-94; PMID:19773794; http://dx.doi.org/10.1038/icb. 2009.69.
55. Xing Z, Lu C, Hu D, Miclau T, 3rd, Marcucio RS. Rejuvenation of the inflammatory system stimulates fracture repair in aged mice. J Orthop Res 2010; 28:1000-6; PMID:20108320.
56. Sopko NA, Turturice BA, Becker ME, Brown CR, Dong F, Popoviæ ZB, et al. Bone marrow support of the heart in pressure overload is lost with aging. PLoS One 2010; 5:15187; PMID:21203577; http://dx.doi.org/10.1371/journal.pone. 0015187.
57. Finerty JC. Parabiosis in physiological studies. Physiol Rev 1952; 32:277-302; PMID:12983225.
58. Bert P. Expériences et Considérations Sur la Greffe Animale. Journal del al Anatomie et de la Physiologie 1864; 1:69-87.
59. McCay CM, Pope F, Lunsford W, Sperling G, Sambhavaphol P. Parabiosis between old and young rats. Gerontologia 1957; 1:7-17; PMID:13405201; http://dx.doi.org/10.1159/000210677.
60. Ludwig FC, Elashoff RM. Mortality in syngeneic rat parabionts of different chronological age. Trans NY Acad Sci 1972; 34:582-7; PMID:4507935.
61. Niikura Y, Niikura T, Wang N, Satirapod C, Tilly JL. Systemic signals in aged males exert potent rejuvenating effects on the ovarian follicle reserve in mammalian females. Aging (Albany NY) 2010; 2:999-1003; PMID:21212462.
62. Song Z, Wang J, Guachalla LM, Terszowski G, Rodewald HR, Ju Z, et al. Alterations of the systemic environment are the primary cause of impaired B and T lymphopoiesis in telomere-dysfunctional mice. Blood 2010; 115:1481-9; PMID:19965646; http://dx.doi.org/10.1182/blood-2009-08-237230.