Stochastic modeling reveals an evolutionary mechanism underlying elevated rates of childhood leukemia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 4, 2016, Pages 1050-1055

  Rozhok, Andrii I ^a   Salstrom, Jennifer L ^a,b   DeGregori, James ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b University of Colorado Denver and Children s Hospital Colorado   (United States)

Author keywords

Aging; Cancer; Childhood leukemia; Somatic evolution; Stochastic modeling

Indexed keywords

ADULT; ARTICLE; CHILD; CHILDHOOD LEUKEMIA; CLONAL EVOLUTION; GENE MUTATION; HEMATOPOIETIC STEM CELL; HUMAN; LEUKEMOGENESIS; MONTE CARLO METHOD; PRIORITY JOURNAL; STOCHASTIC MODEL; AGE; LEUKEMIA; MARKOV CHAIN; MUTATION; PHYSIOLOGY;

AGE FACTORS; CHILD; CLONAL EVOLUTION; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKEMIA; MUTATION; STOCHASTIC PROCESSES;

EID: 84955457039     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1509333113     Document Type: Article

References (47)

1. Armitage P (1985) Multistage models of carcinogenesis. Environ Health Perspect 63: 195-201.
2. Nowell PC (1976) The clonal evolution of tumor cell populations. Science 194(4260): 23-28.
3. Reiter JG, Bozic I, Allen B, Chatterjee K, Nowak MA (2013) The effect of one additional driver mutation on tumor progression. Evol Appl 6(1):34-45.
4. Vogelstein B, et al. (2013) Cancer genome landscapes. Science 339(6127):1546-1558.
5. Gillies RJ, Verduzco D, Gatenby RA (2012) Evolutionary dynamics of carcinogenesis and why targeted therapy does not work. Nat Rev Cancer 12(7):487-493.
6. Henry CJ, Marusyk A, Zaberezhnyy V, Adane B, DeGregori J (2010) Declining lymphoid progenitor fitness promotes aging-associated leukemogenesis. Proc Natl Acad Sci USA 107(50):21713-21718.
7. Marusyk A, et al. (2009) Irradiation alters selection for oncogenic mutations in hematopoietic progenitors. Cancer Res 69(18):7262-7269.
8. Marusyk A, DeGregori J (2008) Declining cellular fitness with age promotes cancer initiation by selecting for adaptive oncogenic mutations. Biochim Biophys Acta 1785(1):1-11.
9. Marusyk A, Porter CC, Zaberezhnyy V, DeGregori J (2010) Irradiation selects for p53-deficient hematopoietic progenitors. PLoS Biol 8(3):e1000324.
10. Vermeulen L, et al. (2013) Defining stem cell dynamics in models of intestinal tumor initiation. Science 342(6161):995-998.
11. Bondar T, Medzhitov R (2010) p53-mediated hematopoietic stem and progenitor cell competition. Cell Stem Cell 6(4):309-322.
12. Bissell MJ, Hines WC (2011) Why don't we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med 17(3):320-329.
13. Wright S (1931) Evolution in Mendelian Populations. Genetics 16(2):97-159.
14. Snippert HJ, et al. (2010) Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 143(1):134-144.
15. Lopez-Garcia C, Klein AM, Simons BD, Winton DJ (2010) Intestinal stem cell replacement follows a pattern of neutral drift. Science 330(6005):822-825.
16. Abkowitz JL, Catlin SN, McCallie MT, Guttorp P (2002) Evidence that the number of hematopoietic stem cells per animal is conserved in mammals. Blood 100(7): 2665-2667.
17. Catlin SN, Busque L, Gale RE, Guttorp P, Abkowitz JL (2011) The replication rate of human hematopoietic stem cells in vivo. Blood 117(17):4460-4466.
18. Wang JC, Doedens M, Dick JE (1997) Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay. Blood 89(11):3919-3924.
19. Abkowitz JL, Catlin SN, Guttorp P (1996) Evidence that hematopoiesis may be a stochastic process in vivo. Nat Med 2(2):190-197.
20. Rozhok AI, Salstrom JL, DeGregori J (2014) Stochastic modeling indicates that aging and somatic evolution in the hematopoetic system are driven by non-cell-autonomous processes. Aging (Albany, NY) 6(12):1033-1048.
21. Eyre-Walker A, Keightley PD (2007) The distribution of fitness effects of new mutations. Nat Rev Genet 8(8):610-618.
22. Fischer RA (1930) The Genetical Theory of Natural Selection (Clarendon, Oxford).
23. Haldane JBS (1932) The Causes of Evolution (Longmans, Green and Co., London).
24. Genovese G, et al. (2014) Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N Engl J Med 371(26):2477-2487.
25. Jaiswal S, et al. (2014) Age-related clonal hematopoiesis associated with adverse outcomes. N Engl J Med 371(26):2488-2498.
26. McKerrell T, et al.; Understanding Society Scientific Group (2015) Leukemia-associated somatic mutations drive distinct patterns of age-related clonal hemopoiesis. Cell Reports 10(8):1239-1245.
27. Xie M, et al. (2014) Age-related mutations associated with clonal hematopoietic expansion and malignancies. Nat Med 20(12):1472-1478.
28. Jacobs KB, et al. (2012) Detectable clonal mosaicism and its relationship to aging and cancer. Nat Genet 44(6):651-658.
29. Laurie CC, et al. (2012) Detectable clonal mosaicism from birth to old age and its relationship to cancer. Nat Genet 44(6):642-650.
30. Greaves M (2006) Infection, immune responses and the aetiology of childhood leukaemia. Nat Rev Cancer 6(3):193-203.
31. Fialkow PJ, Gartler SM, Yoshida A (1967) Clonal origin of chronic myelocytic leukemia in man. Proc Natl Acad Sci USA 58(4):1468-1471.
32. Jan M, et al. (2012) Clonal evolution of preleukemic hematopoietic stem cells precedes human acute myeloid leukemia. Sci Transl Med 4(149):149ra118.
33. Kikushige Y, et al. (2011) Self-renewing hematopoietic stem cell is the primary target in pathogenesis of human chronic lymphocytic leukemia. Cancer Cell 20(2):246-259.
34. Miyamoto T, Weissman IL, Akashi K (2000) AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci USA 97(13):7521-7526.
35. Shlush LI, et al.; HALT Pan-Leukemia Gene Panel Consortium (2014) Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia. Nature 506(7488): 328-333.
36. Greaves MF, Wiemels J (2003) Origins of chromosome translocations in childhood leukaemia. Nat Rev Cancer 3(9):639-649.
37. Stier S, Cheng T, Dombkowski D, Carlesso N, Scadden DT (2002) Notch1 activation increases hematopoietic stem cell self-renewal in vivo and favors lymphoid over myeloid lineage outcome. Blood 99(7):2369-2378.
38. Rozhok AI, DeGregori J (2015) Toward an evolutionary model of cancer: Considering the mechanisms that govern the fate of somatic mutations. Proc Natl Acad Sci USA 112(29):8914-8921.
39. Pui CH, Robison LL, Look AT (2008) Acute lymphoblastic leukaemia. Lancet 371(9617): 1030-1043.
40. Greaves M (2015) When one mutation is all it takes. Cancer Cell 27(4):433-434.
41. Horvath S (2013) DNA methylation age of human tissues and cell types. Genome Biol 14(10):R115.
42. Gorban AN, Pokidysheva LI, Smirnova EV, Tyukina TA (2011) Law of the Minimum paradoxes. Bull Math Biol 73(9):2013-2044.
43. Sidorov I, Kimura M, Yashin A, Aviv A (2009) Leukocyte telomere dynamics and human hematopoietic stem cell kinetics during somatic growth. Exp Hematol 37(4):514-524.
44. Dykstra B, Olthof S, Schreuder J, Ritsema M, de Haan G (2011) Clonal analysis reveals multiple functional defects of aged murine hematopoietic stem cells. J Exp Med 208(13):2691-2703.
45. Pang WW, et al. (2011) Human bone marrow hematopoietic stem cells are increased in frequency and myeloid-biased with age. Proc Natl Acad Sci USA 108(50):20012-20017.
46. Rossi DJ, et al. (2005) Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 102(26):9194-9199.
47. Cancer Genome Atlas Research Network (2013) Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 368(22):2059-2074.