Mesenchymal Inflammation Drives Genotoxic Stress in Hematopoietic Stem Cells and Predicts Disease Evolution in Human Pre-leukemia

Cell Stem Cell

Volumn 19, Issue 5, 2016, Pages 613-627

  Zambetti, Noemi A ^a   Ping, Zhen ^a   Chen, Si ^a   Kenswil, Keane J G ^a   Mylona, Maria A ^a   Sanders, Mathijs A ^a   Hoogenboezem, Remco M ^a   Bindels, Eric M J ^a   Adisty, Maria N ^a   Van Strien, Paulina M H ^a   van der Leije, Cindy S ^a   Westers, Theresia M ^b   Cremers, Eline M P ^b   Milanese, Chiara ^a   Mastroberardino, Pier G ^a   van Leeuwen, Johannes P T M ^a   van der Eerden, Bram C J ^a   Touw, Ivo P ^a   Kuijpers, Taco W ^c   Kanaar, Roland ^a   van de Loosdrecht, Arjan A ^b   Vogl, Thomas ^d   Raaijmakers, Marc H G P ^a   more..

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

cancer; hematopoietic stem cell; inflammation; leukemia; mesenchymal; microenvironment; myelodysplastic syndrome (MDS); niche; S100A8; shwachman diamond syndrome

Indexed keywords

CALGRANULIN A; CALGRANULIN B; PROTEIN P53; TOLL LIKE RECEPTOR; CRE RECOMBINASE; INTEGRASE; OSTERIX PROTEIN, MOUSE; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PROTEIN; PROTEIN S 100; SBDS PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DEPRESSION; CANCER SUSCEPTIBILITY; CELL STRESS; CONTROLLED STUDY; DNA DAMAGE RESPONSE; GENOTOXICITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN TISSUE; INFLAMMATION; MESENCHYME CELL; MITOCHONDRIAL DNA DISORDER; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRELEUKEMIA; PRIORITY JOURNAL; PROGNOSIS; PROGRESSION FREE SURVIVAL; RNA SEQUENCE; SHWACHMAN SYNDROME; SIGNAL TRANSDUCTION; STEM CELL NICHE; TRANSCRIPTION INITIATION; ABNORMALITIES; ANIMAL; BONE; BONE MARROW DISEASE; DISEASE COURSE; DNA DAMAGE; DNA REPAIR; EXOCRINE PANCREATIC INSUFFICIENCY; GENE DELETION; GENETICS; LEUKEMIA; LIPOMATOSIS; MESENCHYMAL STROMA CELL; METABOLISM; MITOCHONDRION; PATHOLOGY; PRECANCER; RISK FACTOR; TREATMENT OUTCOME;

ANIMALS; BONE AND BONES; BONE MARROW DISEASES; DISEASE PROGRESSION; DNA DAMAGE; DNA REPAIR; EXOCRINE PANCREATIC INSUFFICIENCY; GENE DELETION; HEMATOPOIETIC STEM CELLS; HUMANS; INFLAMMATION; INTEGRASES; LEUKEMIA; LIPOMATOSIS; MESENCHYMAL STROMAL CELLS; MICE; MITOCHONDRIA; OXIDATIVE STRESS; PATHOGEN-ASSOCIATED MOLECULAR PATTERN MOLECULES; PRECANCEROUS CONDITIONS; PROTEINS; RISK FACTORS; S100 PROTEINS; SIGNAL TRANSDUCTION; STEM CELL NICHE; TOLL-LIKE RECEPTORS; TRANSCRIPTION FACTORS; TREATMENT OUTCOME; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84994400050     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.08.021     Document Type: Article

References (65)

1. Aggett, P.J., Cavanagh, N.P.C., Matthew, D.J., Pincott, J.R., Sutcliffe, J., Harries, J.T., Shwachman's syndrome. A review of 21 cases. Arch. Dis. Child. 55 (1980), 331–347.
2. Alter, B.P., Diagnosis, genetics, and management of inherited bone marrow failure syndromes. Hematology (Am. Soc. Hematol. Educ. Program) 1 (2007), 29–39.
3. Ambekar, C., Das, B., Yeger, H., Dror, Y., SBDS-deficiency results in deregulation of reactive oxygen species leading to increased cell death and decreased cell growth. Pediatr. Blood Cancer 55 (2010), 1138–1144.
4. Anders, S., Pyl, P.T., Huber, W., HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics 31 (2015), 166–169.
5. Arranz, L., Sánchez-Aguilera, A., Martín-Pérez, D., Isern, J., Langa, X., Tzankov, A., Lundberg, P., Muntión, S., Tzeng, Y.S., Lai, D.M., et al. Neuropathy of haematopoietic stem cell niche is essential for myeloproliferative neoplasms. Nature 512 (2014), 78–81.
6. Austin, K.M., Gupta, M.L. Jr., Coats, S.A., Tulpule, A., Mostoslavsky, G., Balazs, A.B., Mulligan, R.C., Daley, G., Pellman, D., Shimamura, A., Mitotic spindle destabilization and genomic instability in Shwachman-Diamond syndrome. J. Clin. Invest. 118 (2008), 1511–1518.
7. Ball, H.L., Zhang, B., Riches, J.J., Gandhi, R., Li, J., Rommens, J.M., Myers, J.S., Shwachman-Bodian Diamond syndrome is a multi-functional protein implicated in cellular stress responses. Hum. Mol. Genet. 18 (2009), 3684–3695.
8. Bejar, R., Stevenson, K.E., Caughey, B.A., Abdel-Wahab, O., Steensma, D.P., Galili, N., Raza, A., Kantarjian, H., Levine, R.L., Neuberg, D., et al. Validation of a prognostic model and the impact of mutations in patients with lower-risk myelodysplastic syndromes. J. Clin. Oncol. 30 (2012), 3376–3382.
9. Boocock, G.R., Morrison, J.A., Popovic, M., Richards, N., Ellis, L., Durie, P.R., Rommens, J.M., Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat. Genet. 33 (2003), 97–101.
10. Chen, X., Eksioglu, E.A., Zhou, J., Zhang, L., Djeu, J., Fortenbery, N., Epling-Burnette, P., Van Bijnen, S., Dolstra, H., Cannon, J., et al. Induction of myelodysplasia by myeloid-derived suppressor cells. J. Clin. Invest. 123 (2013), 4595–4611.
11. Chen, S., Zambetti, N.A., Bindels, E.M., Kenswill, K., Mylona, A.M., Adisty, N.M., Hoogenboezem, R.M., Sanders, M.A., Cremers, E.M., Westers, T.M., et al. Massive parallel RNA sequencing of highly purified mesenchymal elements in low-risk MDS reveals tissue-context-dependent activation of inflammatory programs. Leukemia, 2016, 10.1038/leu.2016.91 Published online June 3, 2016.
12. Cheng, P., Corzo, C.A., Luetteke, N., Yu, B., Nagaraj, S., Bui, M.M., Ortiz, M., Nacken, W., Sorg, C., Vogl, T., et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J. Exp. Med. 205 (2008), 2235–2249.
13. Curtin, N.J., DNA repair dysregulation from cancer driver to therapeutic target. Nat. Rev. Cancer 12 (2012), 801–817.
14. ∗, Classification of and risk factors for hematologic complications in a French national cohort of 102 patients with Shwachman-Diamond syndrome. Haematologica 97 (2012), 1312–1319.
15. Finch, A.J., Hilcenko, C., Basse, N., Drynan, L.F., Goyenechea, B., Menne, T.F., González Fernández, A., Simpson, P., D'Santos, C.S., Arends, M.J., et al. Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome. Genes Dev. 25 (2011), 917–929.
16. Flores-Figueroa, E., Varma, S., Montgomery, K., Greenberg, P.L., Gratzinger, D., Distinctive contact between CD34+ hematopoietic progenitors and CXCL12+ CD271+ mesenchymal stromal cells in benign and myelodysplastic bone marrow. Lab. Invest. 92 (2012), 1330–1341.
17. Gañán-Gómez, I., Wei, Y., Starczynowski, D.T., Colla, S., Yang, H., Cabrero-Calvo, M., Bohannan, Z.S., Verma, A., Steidl, U., Garcia-Manero, G., Deregulation of innate immune and inflammatory signaling in myelodysplastic syndromes. Leukemia 29 (2015), 1458–1469.
18. Ginzberg, H., Shin, J., Ellis, L., Morrison, J., Ip, W., Dror, Y., Freedman, M., Heitlinger, L.A., Belt, M.A., Corey, M., et al. Shwachman syndrome: phenotypic manifestations of sibling sets and isolated cases in a large patient cohort are similar. J. Pediatr. 135 (1999), 81–88.
19. Hanoun, M., Zhang, D., Mizoguchi, T., Pinho, S., Pierce, H., Kunisaki, Y., Lacombe, J., Armstrong, S.A., Dührsen, U., Frenette, P.S., Acute myelogenous leukemia-induced sympathetic neuropathy promotes malignancy in an altered hematopoietic stem cell niche. Cell Stem Cell 15 (2014), 365–375.
20. Head, D.R., Jacobberger, J.W., Mosse, C., Jagasia, M., Dupont, W., Goodman, S., Flye, L., Shinar, A., McClintock-Treep, S., Stelzer, G., et al. Innovative analyses support a role for DNA damage and an aberrant cell cycle in myelodysplastic syndrome pathogenesis. Bone Marrow Res., 2011, 2011, 950934.
21. Ito, K., Hirao, A., Arai, F., Takubo, K., Matsuoka, S., Miyamoto, K., Ohmura, M., Naka, K., Hosokawa, K., Ikeda, Y., Suda, T., Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 12 (2006), 446–451.
22. Jaiswal, S., Fontanillas, P., Flannick, J., Manning, A., Grauman, P.V., Mar, B.G., Lindsley, R.C., Mermel, C.H., Burtt, N., Chavez, A., et al. Age-related clonal hematopoiesis associated with adverse outcomes. N. Engl. J. Med. 371 (2014), 2488–2498.
23. Jonkers, J., Meuwissen, R., van der Gulden, H., Peterse, H., van der Valk, M., Berns, A., Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29 (2001), 418–425.
24. Kode, A., Manavalan, J.S., Mosialou, I., Bhagat, G., Rathinam, C.V., Luo, N., Khiabanian, H., Lee, A., Murty, V.V., Friedman, R., et al. Leukaemogenesis induced by an activating β-catenin mutation in osteoblasts. Nature 506 (2014), 240–244.
25. Li, C., Chen, H., Ding, F., Zhang, Y., Luo, A., Wang, M., Liu, Z., A novel p53 target gene, S100A9, induces p53-dependent cellular apoptosis and mediates the p53 apoptosis pathway. Biochem. J. 422 (2009), 363–372.
26. Li, L., Li, M., Sun, C., Francisco, L., Chakraborty, S., Sabado, M., McDonald, T., Gyorffy, J., Chang, K., Wang, S., et al. Altered hematopoietic cell gene expression precedes development of therapy-related myelodysplasia/acute myeloid leukemia and identifies patients at risk. Cancer Cell 20 (2011), 591–605.
27. Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
28. Mäkitie, O., Ellis, L., Durie, P.R., Morrison, J.A., Sochett, E.B., Rommens, J.M., Cole, W.G., Skeletal phenotype in patients with Shwachman-Diamond syndrome and mutations in SBDS. Clin. Genet. 65 (2004), 101–112.
29. Maratheftis, C.I., Andreakos, E., Moutsopoulos, H.M., Voulgarelis, M., Toll-like receptor-4 is up-regulated in hematopoietic progenitor cells and contributes to increased apoptosis in myelodysplastic syndromes. Clin. Cancer Res. 13 (2007), 1154–1160.
30. Marino, S., Vooijs, M., van Der Gulden, H., Jonkers, J., Berns, A., Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum. Genes Dev. 14 (2000), 994–1004.
31. Medyouf, H., Mossner, M., Jann, J.C., Nolte, F., Raffel, S., Herrmann, C., Lier, A., Eisen, C., Nowak, V., Zens, B., et al. Myelodysplastic cells in patients reprogram mesenchymal stromal cells to establish a transplantable stem cell niche disease unit. Cell Stem Cell 14 (2014), 824–837.
32. Murphy, M.P., How mitochondria produce reactive oxygen species. Biochem. J. 417 (2009), 1–13.
33. Owusu-Ansah, E., Yavari, A., Mandal, S., Banerjee, U., Distinct mitochondrial retrograde signals control the G1-S cell cycle checkpoint. Nat. Genet. 40 (2008), 356–361.
34. Peddie, C.M., Wolf, C.R., McLellan, L.I., Collins, A.R., Bowen, D.T., Oxidative DNA damage in CD34+ myelodysplastic cells is associated with intracellular redox changes and elevated plasma tumour necrosis factor-alpha concentration. Br. J. Haematol. 99 (1997), 625–631.
35. Raaijmakers, M.H., Mukherjee, S., Guo, S., Zhang, S., Kobayashi, T., Schoonmaker, J.A., Ebert, B.L., Al-Shahrour, F., Hasserjian, R.P., Scadden, E.O., et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 464 (2010), 852–857.
36. Raiser, D.M., Narla, A., Ebert, B.L., The emerging importance of ribosomal dysfunction in the pathogenesis of hematologic disorders. Leuk. Lymphoma 55 (2014), 491–500.
37. Rawls, A.S., Gregory, A.D., Woloszynek, J.R., Liu, F., Link, D.C., Lentiviral-mediated RNAi inhibition of Sbds in murine hematopoietic progenitors impairs their hematopoietic potential. Blood 110 (2007), 2414–2422.
38. Reimand, J., Kull, M., Peterson, H., Hansen, J., Vilo, J., g:Profiler-a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res. 35 (2007), W193–W200.
39. Reimand, J., Arak, T., Vilo, J., g:Profiler-a web server for functional interpretation of gene lists (2011 update). Nucleic Acids Res. 39 (2011), W307–W315.
40. Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W., Smyth, G.K., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, 2015, e47.
41. Robinson, M.D., McCarthy, D.J., Smyth, G.K., edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 (2010), 139–140.
42. Rossi, D.J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J., Weissman, I.L., Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature 447 (2007), 725–729.
43. Sahin, E., Depinho, R.A., Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464 (2010), 520–528.
44. Schepers, K., Pietras, E.M., Reynaud, D., Flach, J., Binnewies, M., Garg, T., Wagers, A.J., Hsiao, E.C., Passegué, E., Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 13 (2013), 285–299.
45. Schepers, K., Campbell, T.B., Passegué, E., Normal and leukemic stem cell niches: insights and therapeutic opportunities. Cell Stem Cell 16 (2015), 254–267.
46. Schneider, R.K., Schenone, M., Ferreira, M.V., Kramann, R., Joyce, C.E., Hartigan, C., Beier, F., Brümmendorf, T.H., Germing, U., Platzbecker, U., et al. Rps14 haploinsufficiency causes a block in erythroid differentiation mediated by S100A8 and S100A9. Nat. Med. 22 (2016), 288–297.
47. Srikrishna, G., Freeze, H.H., Endogenous damage-associated molecular pattern molecules at the crossroads of inflammation and cancer. Neoplasia 11 (2009), 615–628.
48. Starczynowski, D.T., Kuchenbauer, F., Argiropoulos, B., Sung, S., Morin, R., Muranyi, A., Hirst, M., Hogge, D., Marra, M., Wells, R.A., et al. Identification of miR-145 and miR-146a as mediators of the 5q- syndrome phenotype. Nat. Med. 16 (2010), 49–58.
49. Stowe, D.F., Camara, A.K.S., Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid. Redox Signal. 11 (2009), 1373–1414.
50. Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert, B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Lander, E.S., Mesirov, J.P., Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102 (2005), 15545–15550.
51. Toiviainen-Salo, S., Mäyränpää, M.K., Durie, P.R., Richards, N., Grynpas, M., Ellis, L., Ikegawa, S., Cole, W.G., Rommens, J., Marttinen, E., et al. Shwachman-Diamond syndrome is associated with low-turnover osteoporosis. Bone 41 (2007), 965–972.
52. Tormin, A., Li, O., Brune, J.C., Walsh, S., Schütz, B., Ehinger, M., Ditzel, N., Kassem, M., Scheding, S., CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 117 (2011), 5067–5077.
53. Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L., Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28 (2010), 511–515.
54. Tudpor, K., van der Eerden, B.C., Jongwattanapisan, P., Roelofs, J.J., van Leeuwen, J.P., Bindels, R.J., Hoenderop, J.G., Thrombin receptor deficiency leads to a high bone mass phenotype by decreasing the RANKL/OPG ratio. Bone 72 (2015), 14–22.
55. Vlachos, A., Rosenberg, P.S., Atsidaftos, E., Alter, B.P., Lipton, J.M., Incidence of neoplasia in Diamond Blackfan anemia: a report from the Diamond Blackfan Anemia Registry. Blood 119 (2012), 3815–3819.
56. Vogl, T., Tenbrock, K., Ludwig, S., Leukert, N., Ehrhardt, C., van Zoelen, M.A., Nacken, W., Foell, D., van der Poll, T., Sorg, C., Roth, J., Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat. Med. 13 (2007), 1042–1049.
57. Vogl, T., Eisenblätter, M., Völler, T., Zenker, S., Hermann, S., van Lent, P., Faust, A., Geyer, C., Petersen, B., Roebrock, K., et al. Alarmin S100A8/S100A9 as a biomarker for molecular imaging of local inflammatory activity. Nat. Commun., 5, 2014, 4593.
58. Walkley, C.R., Olsen, G.H., Dworkin, S., Fabb, S.A., Swann, J., McArthur, G.A., Westmoreland, S.V., Chambon, P., Scadden, D.T., Purton, L.E., A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell 129 (2007), 1097–1110.
59. Walter, D., Lier, A., Geiselhart, A., Thalheimer, F.B., Huntscha, S., Sobotta, M.C., Moehrle, B., Brocks, D., Bayindir, I., Kaschutnig, P., et al. Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells. Nature 520 (2015), 549–552.
60. Wang, X., Kua, H.Y., Hu, Y., Guo, K., Zeng, Q., Wu, Q., Ng, H.H., Karsenty, G., de Crombrugghe, B., Yeh, J., Li, B., p53 functions as a negative regulator of osteoblastogenesis, osteoblast-dependent osteoclastogenesis, and bone remodeling. J. Cell Biol. 172 (2006), 115–125.
61. Wei, Y., Dimicoli, S., Bueso-Ramos, C., Chen, R., Yang, H., Neuberg, D., Pierce, S., Jia, Y., Zheng, H., Wang, H., et al. Toll-like receptor alterations in myelodysplastic syndrome. Leukemia 27 (2013), 1832–1840.
62. Woloszynek, J.R., Rothbaum, R.J., Rawls, A.S., Minx, P.J., Wilson, R.K., Mason, P.J., Bessler, M., Link, D.C., Mutations of the SBDS gene are present in most patients with Shwachman-Diamond syndrome. Blood 104 (2004), 3588–3590.
63. Xiao, Y., Wang, J., Song, H., Zou, P., Zhou, D., Liu, L., CD34+ cells from patients with myelodysplastic syndrome present different p21 dependent premature senescence. Leuk. Res. 37 (2013), 333–340.
64. Yahata, T., Takanashi, T., Muguruma, Y., Ibrahim, A.A., Matsuzawa, H., Uno, T., Sheng, Y., Onizuka, M., Ito, M., Kato, S., Ando, K., Accumulation of oxidative DNA damage restricts the self-renewal capacity of human hematopoietic stem cells. Blood 118 (2011), 2941–2950.
65. Zambetti, N.A., Bindels, E.M., Van Strien, P.M., Valkhof, M.G., Adisty, M.N., Hoogenboezem, R.M., Sanders, M.A., Rommens, J.M., Touw, I.P., Raaijmakers, M.H., Deficiency of the ribosome biogenesis gene Sbds in hematopoietic stem and progenitor cells causes neutropenia in mice by attenuating lineage progression in myelocytes. Haematologica 100 (2015), 1285–1293.