Human and murine hematopoietic stem cell aging is associated with functional impairments and intrinsic megakaryocytic/erythroid bias

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Nilsson, Alexandra Rundberg ^a,b   Soneji, Shamit ^a,b   Adolfsson, Sofia ^a,b   Bryder, David ^a,b   Pronk, Cornelis Jan ^a,b,c  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AGE; ANIMAL CELL; ARTICLE; BONE MARROW; CELL AGING; CELL PROLIFERATION; ERYTHROCYTE; FUNCTIONAL DISEASE; GENE EXPRESSION; GRANULOCYTE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LYMPHOID PROGENITOR CELL; MACROPHAGE; MEGAKARYOCYTE; MOUSE; NONHUMAN; UMBILICAL CORD BLOOD; ADULT; ANIMAL; CELL LINEAGE; CYTOLOGY; ERYTHROID CELL; FEMALE; GENETIC TRANSCRIPTION; PHENOTYPE; YOUNG ADULT;

ADULT; ANIMALS; CELL AGING; CELL LINEAGE; ERYTHROID CELLS; FEMALE; HEMATOPOIETIC STEM CELLS; HUMANS; MEGAKARYOCYTES; MICE; PHENOTYPE; TRANSCRIPTION, GENETIC; YOUNG ADULT;

EID: 84978086032     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158369     Document Type: Article

References (63)

1. Burch JB, Augustine AD, Frieden LA, Hadley E, Howcroft TK, Johnson R, et al. Advances in geroscience: impact on healthspan and chronic disease. The journals of gerontology Series A, Biological sciences and medical sciences. 2014; 69 Suppl 1:S1-3. doi: 10.1093/gerona/glu041 PMID: 24833579; PubMed Central PMCID: PMC4036419.
2. Boraschi D, Aguado MT, Dutel C, Goronzy J, Louis J, Grubeck-Loebenstein B, et al. The gracefully aging immune system. Science translational medicine. 2013; 5(185):185ps8. doi: 10.1126/scitranslmed.3005624 PMID: 23677590.
3. Berliner N. Anemia in the elderly. Transactions of the American Clinical and Climatological Association. 2013; 124:230-7. PMID: 23874029; PubMed Central PMCID: PMC3715932.
4. Ferrucci L, Balducci L. Anemia of aging: the role of chronic inflammation and cancer. Seminars in hematology. 2008; 45(4):242-9. doi: 10.1053/j.seminhematol.2008.06.001 PMID: 18809094; PubMed Central PMCID: PMC2645640.
5. Lichtman MA, Rowe JM. The relationship of patient age to the pathobiology of the clonal myeloid diseases. Seminars in oncology. 2004; 31(2):185-97. PMID: 15112149.
6. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell. 2008; 132(4):681-96. Epub 2008/02/26. S0092-8674(08)00137-2 [pii] doi: 10.1016/j.cell.2008.01.036 PMID: 18295583.
7. Naveiras O, Nardi V, Wenzel PL, Hauschka PV, Fahey F, Daley GQ. Bone-marrow adipocytes as negative regulators of the haematopoietic microenvironment. Nature. 2009; 460(7252):259-63. doi: 10.1038/nature08099 PMID: 19516257; PubMed Central PMCID: PMC2831539.
8. Vas V, Senger K, Dorr K, Niebel A, Geiger H. Aging of the microenvironment influences clonality in hematopoiesis. PloS one. 2012; 7(8):e42080. doi: 10.1371/journal.pone.0042080 PMID: 22879906; PubMed Central PMCID: PMC3412859.
9. Kusumbe AP, Ramasamy SK, Itkin T, Mae MA, Langen UH, Betsholtz C, et al. Age-dependent modulation of vascular niches for haematopoietic stem cells. Nature. 2016; 532(7599):380-4. doi: 10.1038/nature17638 PMID: 27074508.
10. Kim M, Moon HB, Spangrude GJ. Major age-related changes of mouse hematopoietic stem/progenitor cells. Annals of the New York Academy of Sciences. 2003; 996:195-208. PMID: 12799297.
11. Chambers SM, Shaw CA, Gatza C, Fisk CJ, Donehower LA, Goodell MA. Aging hematopoietic stem cells decline in function and exhibit epigenetic dysregulation. PLoS biology. 2007; 5(8):e201. doi: 10.1371/journal.pbio.0050201 PMID: 17676974; PubMed Central PMCID: PMC1925137.
12. Rossi DJ, Bryder D, Zahn JM, Ahlenius H, Sonu R, Wagers AJ, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci U S A. 2005; 102(26):9194-9. Epub 2005/06/22.0503280102 [pii] doi: 10.1073/pnas.0503280102 PMID: 15967997; PubMed Central PMCID: PMC1153718.
13. Wahlestedt M, Norddahl GL, Sten G, Ugale A, Frisk MA, Mattsson R, et al. An epigenetic component of hematopoietic stem cell aging amenable to reprogramming into a young state. Blood. 2013; 121(21):4257-64. doi: 10.1182/blood-2012-11-469080 PMID: 23476050.
14. Dykstra B, Olthof S, Schreuder J, Ritsema M, de Haan G. Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. The Journal of experimental medicine. 2011; 208(13):2691-703. doi: 10.1084/jem.20111490 PMID: 22110168; PubMed Central PMCID: PMC3244040.
15. Beerman I, Bhattacharya D, Zandi S, Sigvardsson M, Weissman IL, Bryder D, et al. Functionally distinct hematopoietic stem cells modulate hematopoietic lineage potential during aging by a mechanism of clonal expansion. Proceedings of the National Academy of Sciences of the United States of America. 2010; 107(12):5465-70. doi: 10.1073/pnas.1000834107 PMID: 20304793; PubMed Central PMCID: PMC2851806.
16. Beerman I, Bock C, Garrison BS, Smith ZD, Gu H, Meissner A, et al. Proliferation-dependent alterations of the DNA methylation landscape underlie hematopoietic stem cell aging. Cell stem cell. 2013; 12(4):413-25. doi: 10.1016/j.stem.2013.01.017 PMID: 23415915.
17. Morrison SJ, Wandycz AM, Akashi K, Globerson A, Weissman IL. The aging of hematopoietic stem cells. Nature medicine. 1996; 2(9):1011-6. PMID: 8782459.
18. Cho RH, Sieburg HB, Muller-Sieburg CE. A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells. Blood. 2008; 111(12):5553-61. doi: 10.1182/blood-2007-11-123547 PMID: 18413859; PubMed Central PMCID: PMC2424153.
19. Morita Y, Ema H, Nakauchi H. Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. The Journal of experimental medicine. 2010; 207(6):1173-82. doi: 10.1084/jem.20091318 PMID: 20421392; PubMed Central PMCID: PMC2882827.
20. Muller-Sieburg C, Sieburg HB. Stem cell aging: survival of the laziest? Cell cycle. 2008; 7(24):3798-804. PMID: 19066464; PubMed Central PMCID: PMC2746656.
21. Grover A, Sanjuan-Pla A, Thongjuea S, Carrelha J, Giustacchini A, Gambardella A, et al. Single-cell RNA sequencing reveals molecular and functional platelet bias of aged haematopoietic stem cells. Nat Commun. 2016; 7:11075. doi: 10.1038/ncomms11075 PMID: 27009448; PubMed Central PMCID: PMCPMC4820843.
22. Gale RE, Fielding AK, Harrison CN, Linch DC. Acquired skewing of X-chromosome inactivation patterns in myeloid cells of the elderly suggests stochastic clonal loss with age. British journal of haematology. 1997; 98(3):512-9. PMID: 9332303.
23. Lansdorp PM, Dragowska W, Mayani H. Ontogeny-related changes in proliferative potential of human hematopoietic cells. The Journal of experimental medicine. 1993; 178(3):787-91. PMID: 7688789; PubMed Central PMCID: PMC2191172.
24. Marley SB, Lewis JL, Davidson RJ, Roberts IA, Dokal I, Goldman JM, et al. Evidence for a continuous decline in haemopoietic cell function from birth: application to evaluating bone marrow failure in children. British journal of haematology. 1999; 106(1):162-6. PMID: 10444180.
25. Finke J, Schmoor C, Bethge WA, Ottinger HD, Stelljes M, Zander AR, et al. Prognostic factors affecting outcome after allogeneic transplantation for hematological malignancies from unrelated donors: results from a randomized trial. Biology of blood and marrow transplantation: journal of the American Society for Blood and Marrow Transplantation. 2012; 18(11):1716-26. doi: 10.1016/j.bbmt.2012.06.001 PMID: 22713691.
26. Heining C, Spyridonidis A, Bernhardt E, Schulte-Monting J, Behringer D, Grullich C, et al. Lymphocyte reconstitution following allogeneic hematopoietic stem cell transplantation: a retrospective study including 148 patients. Bone marrow transplantation. 2007; 39(10):613-22. doi: 10.1038/sj.bmt.1705648 PMID: 17384658.
27. Kollman C, Howe CW, Anasetti C, Antin JH, Davies SM, Filipovich AH, et al. Donor characteristics as risk factors in recipients after transplantation of bone marrow from unrelated donors: the effect of donor age. Blood. 2001; 98(7):2043-51. PMID: 11567988.
28. Woolthuis CM, Mariani N, Verkaik-Schakel RN, Brouwers-Vos AZ, Schuringa JJ, Vellenga E, et al. Aging impairs long-term hematopoietic regeneration after autologous stem cell transplantation. Biology of blood and marrow transplantation: journal of the American Society for Blood and Marrow Transplantation. 2014; 20(6):865-71. doi: 10.1016/j.bbmt.2014.03.001 PMID: 24607555.
29. Wahlestedt M, Pronk CJ, Bryder D. Concise review: hematopoietic stem cell aging and the prospects for rejuvenation. Stem cells translational medicine. 2015; 4(2):186-94. doi: 10.5966/sctm.2014-0132 PMID: 25548388; PubMed Central PMCID: PMC4303356.
30. Pang WW, Price EA, Sahoo D, Beerman I, Maloney WJ, Rossi DJ, et al. Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proceedings of the National Academy of Sciences of the United States of America. 2011; 108(50):20012-7. doi: 10.1073/pnas.1116110108 PMID: 22123971; PubMed Central PMCID: PMC3250139.
31. Kuranda K, Vargaftig J, de la Rochere P, Dosquet C, Charron D, Bardin F, et al. Age-related changes in human hematopoietic stem/progenitor cells. Aging cell. 2011; 10(3):542-6. doi: 10.1111/j.1474-9726.2011.00675.x PMID: 21418508.
32. Pronk CJ, Rossi DJ, Mansson R, Attema JL, Norddahl GL, Chan CK, et al. Elucidation of the phenotypic, functional, and molecular topography of a myeloerythroid progenitor cell hierarchy. Cell stem cell. 2007; 1(4):428-42. doi: 10.1016/j.stem.2007.07.005 PMID: 18371379.
33. Pronk CJ, Bryder D. Flow cytometry-based identification of immature myeloerythroid development. Methods in molecular biology. 2011; 699:275-93. doi: 10.1007/978-1-61737-950-5-13 PMID: 21116988.
34. Norddahl GL, Wahlestedt M, Gisler S, Sigvardsson M, Bryder D. Reduced repression of cytokine signaling ameliorates age-induced decline in hematopoietic stem cell function. Aging cell. 2012; 11(6):1128-31. doi: 10.1111/j.1474-9726.2012.00863.x PMID: 22809070.
35. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4(2):249-64. doi: 10.1093/biostatistics/4.2.249 PMID: 12925520.
36. Wettenhall JM, Smyth GK. limmaGUI: a graphical user interface for linear modeling of microarray data. Bioinformatics. 2004; 20(18):3705-6. doi: 10.1093/bioinformatics/bth449 PMID: 15297296.
37. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proceedings of the National Academy of Sciences of the United States of America. 2005; 102(43):15545-50. doi: 10.1073/pnas.0506580102 PMID: 16199517; PubMed Central PMCID: PMC1239896.
38. Spinelli L, Carpentier S, Montanana Sanchis F, Dalod M, Vu Manh TP. BubbleGUM: automatic extraction of phenotype molecular signatures and comprehensive visualization of multiple Gene Set Enrichment Analyses. BMC Genomics. 2015; 16(1):814. doi: 10.1186/s12864-015-2012-4 PMID: 26481321; PubMed Central PMCID: PMCPMC4617899.
39. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols. 2009; 4(1):44-57. doi: 10.1038/nprot.2008.211 PMID: 19131956.
40. Yates A, Akanni W, Amode MR, Barrell D, Billis K, Carvalho-Silva D, et al. Ensembl 2016. Nucleic Acids Res. 2016; 44(D1):D710-6. doi: 10.1093/nar/gkv1157 PMID: 26687719; PubMed Central PMCID: PMCPMC4702834.
41. Craig W, Kay R, Cutler RL, Lansdorp PM. Expression of Thy-1 on human hematopoietic progenitor cells. The Journal of experimental medicine. 1993; 177(5):1331-42. PMID: 7683034; PubMed Central PMCID: PMC2191025.
42. Notta F, Doulatov S, Laurenti E, Poeppl A, Jurisica I, Dick JE. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science. 2011; 333(6039):218-21. doi: 10.1126/science.1201219 PMID: 21737740.
43. Petzer AL, Hogge DE, Landsdorp PM, Reid DS, Eaves CJ. Self-renewal of primitive human hematopoietic cells (long-term-culture-initiating cells) in vitro and their expansion in defined medium. Proceedings of the National Academy of Sciences of the United States of America. 1996; 93(4):1470-4. PMID: 8643656; PubMed Central PMCID: PMC39963.
44. Edvardsson L, Dykes J, Olofsson T. Isolation and characterization of human myeloid progenitor populations - TpoR as discriminator between common myeloid and megakaryocyte/erythroid progenitors. Experimental hematology. 2006; 34(5):599-609. doi: 10.1016/j.exphem.2006.01.017 PMID: 16647566.
45. Hao QL, Zhu J, Price MA, Payne KJ, Barsky LW, Crooks GM. Identification of a novel, human multilymphoid progenitor in cord blood. Blood. 2001; 97(12):3683-90. PMID: 11389003.
46. Manz MG, Miyamoto T, Akashi K, Weissman IL. Prospective isolation of human clonogenic common myeloid progenitors. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99(18):11872-7. doi: 10.1073/pnas.172384399 PMID: 12193648; PubMed Central PMCID: PMC129361.
47. Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005; 121(7):1109-21. doi: 10.1016/j.cell.2005.05.026 PMID: 15989959.
48. Karsunky H, Inlay MA, Serwold T, Bhattacharya D, Weissman IL. Flk2+ common lymphoid progenitors possess equivalent differentiation potential for the B and T lineages. Blood. 2008; 111(12):5562-70. doi: 10.1182/blood-2007-11-126219 PMID: 18424665; PubMed Central PMCID: PMCPMC2424154.
49. Biino G, Santimone I, Minelli C, Sorice R, Frongia B, Traglia M, et al. Age- and sex-related variations in platelet count in Italy: a proposal of reference ranges based on 40987 subjects' data. PloS one. 2013; 8(1):e54289. doi: 10.1371/journal.pone.0054289 PMID: 23382888; PubMed Central PMCID: PMC3561305.
50. Sanjuan-Pla A, Macaulay IC, Jensen CT, Woll PS, Luis TC, Mead A, et al. Platelet-biased stem cells reside at the apex of the haematopoietic stem-cell hierarchy. Nature. 2013; 502(7470):232-6. doi: 10.1038/nature12495 PMID: 23934107.
51. van Galen P, Kreso A, Wienholds E, Laurenti E, Eppert K, Lechman ER, et al. Reduced lymphoid lineage priming promotes human hematopoietic stem cell expansion. Cell stem cell. 2014; 14(1):94-106. doi: 10.1016/j.stem.2013.11.021 PMID: 24388174.
52. Umemoto T, Yamato M, Shiratsuchi Y, Terasawa M, Yang J, Nishida K, et al. CD61 enriches long-term repopulating hematopoietic stem cells. Biochem Biophys Res Commun. 2008; 365(1):176-82. doi: 10.1016/j.bbrc.2007.10.168 PMID: 17983596.
53. Sun D, Luo M, Jeong M, Rodriguez B, Xia Z, Hannah R, et al. Epigenomic profiling of young and aged HSCs reveals concerted changes during aging that reinforce self-renewal. Cell stem cell. 2014; 14(5):673-88. doi: 10.1016/j.stem.2014.03.002 PMID: 24792119; PubMed Central PMCID: PMCPMC4070311.
54. Bernal-Quiros M, Wu YY, Alarcon-Riquelme ME, Castillejo-Lopez C. BANK1 and BLK act through phospholipase C gamma 2 in B-cell signaling. PloS one. 2013; 8(3):e59842. doi: 10.1371/journal.pone.0059842 PMID: 23555801; PubMed Central PMCID: PMCPMC3608554.
55. Banerjee ER, Latchman YE, Jiang Y, Priestley GV, Papayannopoulou T. Distinct changes in adult lymphopoiesis in Rag2-/- mice fully reconstituted by alpha4-deficient adult bone marrow cells. Experimental hematology. 2008; 36(8):1004-13. doi: 10.1016/j.exphem.2008.03.008 PMID: 18468770; PubMed Central PMCID: PMCPMC3705905.
56. Sudo K, Ema H, Morita Y, Nakauchi H. Age-associated characteristics of murine hematopoietic stem cells. J Exp Med. 2000; 192(9):1273-80. Epub 2000/11/09. PMID: 11067876; PubMed Central PMCID: PMC2193349.
57. Taraldsrud E, Grogaard HK, Solheim S, Lunde K, Floisand Y, Arnesen H, et al. Age and stress related phenotypical changes in bone marrow CD34+ cells. Scandinavian journal of clinical and laboratory investigation. 2009; 69(1):79-84. doi: 10.1080/00365510802419447 PMID: 18836945.
58. Notta F, Zandi S, Takayama N, Dobson S, Gan OI, Wilson G, et al. Distinct routes of lineage development reshape the human blood hierarchy across ontogeny. Science. 2016; 351(6269):aab2116. doi: 10.1126/science.aab2116 PMID: 26541609; PubMed Central PMCID: PMCPMC4816201.
59. Mori Y, Chen JY, Pluvinage JV, Seita J, Weissman IL. Prospective isolation of human erythroid lineage-committed progenitors. Proceedings of the National Academy of Sciences of the United States of America. 2015; 112(31):9638-43. doi: 10.1073/pnas.1512076112 PMID: 26195758; PubMed Central PMCID: PMCPMC4534255.
60. Price EA. Aging and erythropoiesis: current state of knowledge. Blood Cells Mol Dis. 2008; 41(2):158-65. doi: 10.1016/j.bcmd.2008.04.005 PMID: 18514554.
61. Balduini CL, Noris P. Platelet count and aging. Haematologica. 2014; 99(6):953-5. doi: 10.3324/haematol.2014.106260 PMID: 24881040; PubMed Central PMCID: PMC4040891.
62. Xing Z, Ryan MA, Daria D, Nattamai KJ, Van Zant G, Wang L, et al. Increased hematopoietic stem cell mobilization in aged mice. Blood. 2006; 108(7):2190-7. doi: 10.1182/blood-2005-12-010272 PMID: 16741255; PubMed Central PMCID: PMCPMC1895568.
63. Verovskaya E, Broekhuis MJ, Zwart E, Ritsema M, van Os R, de Haan G, et al. Heterogeneity of young and aged murine hematopoietic stem cells revealed by quantitative clonal analysis using cellular barcoding. Blood. 2013; 122(4):523-32. doi: 10.1182/blood-2013-01-481135 PMID: 23719303.