Coordinate regulation of residual bone marrow function by paracrine trafficking of AML exosomes

Leukemia

Volumn 29, Issue 12, 2015, Pages 2285-2295

  Huan, J ^a   Hornick, N I ^a   Goloviznina, N A ^a   Kamimae Lanning, A N ^a   David, L L ^a   Wilmarth, P A ^a   Mori, T ^a   Chevillet, J R ^b   Narla, A ^c   Roberts, C T ^a,d,e   Loriaux, M M ^a,d   Chang, B H ^a   Kurre, P ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b USA   (United States)

^c STANFORD UNIVERSITY   (United States)

^d OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE MYELOID LEUKEMIA; ANIMAL; BONE MARROW; C57BL MOUSE; CELL MOTION; EXOSOME; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HL-60 CELL LINE; HUMAN; MOUSE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BONE MARROW; CELL MOVEMENT; EXOSOMES; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HL-60 CELLS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED C57BL;

EID: 84951569690     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2015.163     Document Type: Article

References (47)

1. Ayala F, Dewar R, Kieran M, Kalluri R. Contribution of bone microenvironment to leukemogenesis and leukemia progression. Leukemia 2009; 23: 2233-2241.
2. Reynaud D, Pietras E, Barry-Holson K, Mir A, Binnewies M, Jeanne M, et al. IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development. Cancer Cell 2011; 20: 661-673.
3. Zhang B, Ho YW, Huang Q, Maeda T, Lin A, Lee SU, et al. Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 2012; 21: 577-592.
4. Miraki-Moud F, Anjos-Afonso F, Hodby KA, Griessinger E, Rosignoli G, Lillington D, et al. Acute myeloid leukemia does not deplete normal hematopoietic stem cells but induces cytopenias by impeding their differentiation. Proc Natl Acad Sci USA 2013; 110: 13576-13581.
5. Colmone A, Amorim M, Pontier AL, Wang S, Jablonski E, Sipkins DA. Leukemic cells create bone marrow niches that disrupt the behavior of normal hematopoietic progenitor cells. Science 2008; 322: 1861-1865.
6. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, et al. Embryonic stem cell-Derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006; 20: 847-856.
7. Huan J, Hornick NI, Shurtleff MJ, Skinner AM, Goloviznina NA, Roberts CT Jr, et al. RNA trafficking by acute myelogenous leukemia exosomes. Cancer Res 2013; 73: 918-929.
8. Chen Y, Jacamo R, Konopleva M, Garzon R, Croce C, Andreeff M. CXCR4 downregulation of let-7a drives chemoresistance in acute myeloid leukemia. J Clin Invest 2013; 123: 2395-2407.
9. Roberts Jr. CT, Kurre P. Vesicle trafficking and RNA transfer add complexity and connectivity to cell-cell communication. Cancer Res 2013; 73: 3200-3205.
10. Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood 2002; 99: 394.
11. Hatfield KJ, Bedringsaas SL, Ryningen A, Gjertsen BT, Bruserud O. Hypoxia increases HIF-1alpha expression and constitutive cytokine release by primary human acute myeloid leukaemia cells. Eur Cyt Netw 2010; 21: 154-164.
12. Lam BS, Adams GB. Blocking HIF1alpha activity eliminates hematological cancer stem cells. Cell Stem Cell 2011; 8: 354-356.
13. Chen Y, Jacamo R, Shi YX, Wang RY, Battula VL, Konoplev S, et al. Human extramedullary bone marrow in mice: a novel in vivo model of genetically controlled hematopoietic microenvironment. Blood 2012; 119: 4971-4980.
14. Pan D. In situ (in vivo) gene transfer into murine bone marrow stem cells. Methods Mol Biol 2009; 506: 159-169.
15. Mazurier F, Doedens M, Gan OI, Dick JE. Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med 2003; 9: 959-963.
16. Skinner AM, Grompe M, Kurre P. Intra-hematopoietic cell fusion as a source of somatic variation in the hematopoietic system. J Cell Sci 2012; 125: 2837-2843.
17. Wilmarth PA, Tanner S, Dasari S, Nagalla SR, Riviere MA, Bafna V, et al. Age-related changes in human crystallins determined from comparative analysis of posttranslational modifications in young and aged lens: does deamidation contribute to crystallin insolubility?. J Proteome Res 2006; 5: 2554-2566.
18. McAlister GC, Huttlin EL, Haas W, Ting L, Jedrychowski MP, Rogers JC, et al. Increasing the multiplexing capacity of TMTs using reporter ion isotopologues with isobaric masses. Anal Chem 2012; 84: 7469-7478.
19. Kall L, Canterbury JD, Weston J, Noble WS, MacCoss MJ. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods 2007; 4: 923-925.
20. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 2010; 26: 139-140.
21. Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxiadependent activation of vascular cells during tumor development. Proc Natl Acad Sci USA 2013; 110: 7312-7317.
22. Schepers K, Pietras EM, Reynaud D, Flach J, Binnewies M, Garg T, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a selfreinforcing leukemic niche. Cell Stem Cell 2013; 13: 285-299.
23. Ghosh AK, Shanafelt TD, Cimmino A, Taccioli C, Volinia S, Liu CG, et al. Aberrant regulation of pVHL levels by microRNA promotes the HIF/VEGF axis in CLL B cells. Blood 2009; 113: 5568-5574.
24. Ohno Y, Yasunaga S, Janmohamed S, Ohtsubo M, Saeki K, Kurogi T, et al. Hoxa9 transduction induces hematopoietic stem and progenitor cell activity through direct down-regulation of geminin protein. PloS One 2013; 8: e53161.
25. Chong JL, Tsai SY, Sharma N, Opavsky R, Price R, Wu L, et al. E2f3a and E2f3b contribute to the control of cell proliferation and mouse development. Mol Cell Biol 2009; 29: 414-424.
26. Sattler M, Verma S, Pride YB, Salgia R, Rohrschneider LR, Griffin JD. SHIP1 an SH2 domain containing polyinositol-5-phosphatase, regulates migration through two critical tyrosine residues and forms a novel signaling complex with DOK1 and CRKL. J Biol Chem 2001; 276: 2451-2458.
27. Huang X, Ding L, Bennewith KL, Tong RT, Welford SM, Ang KK, et al. Hypoxiainducible mir-210 regulates normoxic gene expression involved in tumor initiation. Mol Cell 2009; 35: 856-867.
28. Lee DW, Futami M, Carroll M, Feng Y, Wang Z, Fernandez M, et al. Loss of SHIP-1 protein expression in high-risk myelodysplastic syndromes is associated with miR-210 and miR-155. Oncogene 2012; 31: 4085-4094.
29. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 2007; 131: 146-159.
30. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
31. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37: 1-13.
32. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, et al. STRING 8-A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009; 37: D412-D416.
33. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F, Dick JE. Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 2006; 12: 1167-1174.
34. Jacamo R, Chen Y, Wang Z, Ma W, Zhang M, Spaeth EL, et al. Reciprocal leukemiastroma VCAM-1/VLA-4-Dependent activation of NF-kappaB mediates chemoresistance. Blood 2014; 123: 2691-2702.
35. Mizuno S, Chijiwa T, Okamura T, Akashi K, Fukumaki Y, Niho Y, et al. Expression of DNA methyltransferases DNMT1, 3A, and 3B in normal hematopoiesis and in acute and chronic myelogenous leukemia. Blood 2001; 97: 1172-1179.
36. Sugiyama T, Kohara H, Noda M, Nagasawa T. Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity 2006; 25: 977-988.
37. Cosgun KN, Rahmig S, Mende N, Reinke S, Hauber I, Schafer C, et al. Kit regulates HSC engraftment across the human-mouse species barrier. Cell Stem Cell 2014; 15: 227-238.
38. Greenbaum A, Hsu YM, Day RB, Schuettpelz LG, Christopher MJ, Borgerding JN, et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 2013; 495: 227-230.
39. Mocsai A, Ruland J, Tybulewicz VL. The SYK tyrosine kinase: a crucial player in diverse biological functions. Nat Rev Immunol 2010; 10: 387-402.
40. Puissant A, Fenouille N, Alexe G, Pikman Y, Bassil CF, Mehta S, et al. SYK is a critical regulator of FLT3 in acute myeloid leukemia. Cancer Cell 2014; 25: 226-242.
41. Hahn CK, Berchuck JE, Ross KN, Kakoza RM, Clauser K, Schinzel AC, et al. Proteomic and genetic approaches identify Syk as an AML target. Cancer Cell 2009; 16: 281-294.
42. Gross O, Poeck H, Bscheider M, Dostert C, Hannesschlager N, Endres S, et al. Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 2009; 459: 433-436.
43. Yonemura Y, Ku H, Hirayama F, Souza LM, Ogawa M. Interleukin 3 or interleukin 1 abrogates the reconstituting ability of hematopoietic stem cells. Proc Natl Acad Sci USA 1996; 93: 4040-4044.
44. Hartwig UF, Keller U, Huber C, Peschel C. Regulation of hematopoietic growth factor production by genetically modified human bone marrow stromal cells expressing interleukin-1beta antisense RNA. J Interferon Cytokine Res 2001; 21: 851-860.
45. Signer RA, Magee JA, Salic A, Morrison SJ. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature 2014; 509: 49-54.
46. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a prometastatic phenotype through MET. Nat Med 2012; 18: 883-891.
47. Barcellos-Hoff MH, Lyden D, Wang TC. The evolution of the cancer niche during multistage carcinogenesis. Nat Rev Cancer 2013; 13: 511-518.