The stem cell fitness landscape and pathways of molecular leukemogenesis

Frontiers in Bioscience - Scholar

Volumn 3 S, Issue 2, 2011, Pages 487-500

  Bagby, Grover C ^a,b,c   Fleischman, Angela G ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c PORTLAND VA MEDICAL CENTER   (United States)

Author keywords

Aplastic Anemia; Clonal Evolution; Fanconi Anemia; Hematopoietic Stem Cells; Interferon Gamma; Leukemogenesis; Mutation; Myeloproliferative Diseases; Review; Tumor Necrosis Factor Alpha

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; GAMMA INTERFERON; INTERLEUKIN 6; JANUS KINASE 2; MELANOCORTIN 1 RECEPTOR; PROTEIN KINASE R; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 8; TRANSCRIPTION FACTOR HOXA9; TRANSCRIPTION FACTOR RUNX1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

ACUTE GRANULOCYTIC LEUKEMIA; APLASTIC ANEMIA; BONE MARROW DEPRESSION; BONE MARROW SUPPRESSION; CANCER GROWTH; CANCER PREVENTION; CANCER STEM CELL; CHROMOSOMAL INSTABILITY; CHROMOSOME BREAKAGE; CHROMOSOME DELETION; CLONAL EVOLUTION; CYTOKINE PRODUCTION; DNA CROSS LINKING; DNA DAMAGE; DNA SEQUENCE; FANCONI ANEMIA; HAPLOTYPE; HELICOBACTER INFECTION; HEMATOPOIETIC STEM CELL; HETEROZYGOSITY LOSS; HIGH THROUGHPUT SCREENING; HUMAN; LEUKEMOGENESIS; MISSENSE MUTATION; MOLECULAR PATHOLOGY; MONONUCLEAR PHAGOCYTE; MONOZYGOTIC TWINS; MOSAICISM; MYELODYSPLASTIC SYNDROME; NONHUMAN; ONCOGENE; PERIPHERAL LYMPHOCYTE; PHILADELPHIA CHROMOSOME NEGATIVE CELL; REVIEW; SIGNAL TRANSDUCTION; SOMATIC MUTATION; STEM CELL EXPANSION; T LYMPHOCYTE; BIOLOGICAL MODEL; GENETIC SELECTION; GENETICS; METABOLISM; MUTATION; PAROXYSMAL NOCTURNAL HEMOGLOBINURIA; PATHOLOGY; PHENOTYPE; REPRODUCTIVE FITNESS;

CYTOKINES; GENETIC FITNESS; HEMOGLOBINURIA, PAROXYSMAL; HUMANS; JANUS KINASE 2; LEUKEMIA, MYELOID, ACUTE; MODELS, BIOLOGICAL; MUTATION; MYELODYSPLASTIC SYNDROMES; NEOPLASTIC STEM CELLS; PHENOTYPE; SELECTION, GENETIC;

EID: 79956033992     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: 10.2741/s167     Document Type: Review

References (129)

1. Elaine Mardis, Li Ding, David Dooling, David Larson, Michael McLellan, Ken Chen, Daniel Koboldt, Robert Fulton, Kim Delehaunty, Sean McGrath, Lucinda Fulton, Devin Locke, Vincent Magrini, Rachel Abbott, Tammi Vickery, Jerry Reed, Jody Robinson, Todd Wylie, Scott Smith, Lynn Carmichael, James Eldred, Christopher Harris, Jason Walker, Joshua Peck, Feiyu Du, Adam Dukes, Gabriel Sanderson, Anthony Brummett, Eric Clark, Joshua McMichael, Rick Meyer, Jonathan Schindler, Craig Pohl, John Wallis, Xiaoqi Shi, Ling Lin, Heather Schmidt, Yuzhu Tang, Carrie Haipek, Madeline E. Wiechert, Jolynda V. Ivy, Joelle Kalicki, Glendoria Elliott, Rhonda E. Ries, Jacqueline E. Payton, Peter Westervelt, Michael Tomasson, Mark Watson, Jack Baty, Sharon Heath, William Shannon, Rakesh Nagarajan, Daniel Link, Matthew Walter, Timothy Graubert, John DiPersio, Richard Wilson and Timothy Ley: Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med 361, 1058-1066 (2009)
2. Matthew Walter, Jacqueline Payton, Rhonda Ries, William Shannon, Hrishikesh Deshmukh, Yu Zhao, Jack Baty, Sharon Heath, Peter Westervelt, Mark Watson, Michael Tomasson, Rakesh Nagarajan, Brian O'Gara, Clara Bloomfield, Krzysztof Mrozek, Rebecca Selzer, Todd Richmond, Jacob Kitzman, Joel Geoghegan, Peggy Eis, Rachel Maupin, Robert Fulton, Michael McLellan, Richard Wilson, Elaine Mardis, Daniel Link, Timothy Graubert, John DiPersio and Timothy Ley: Acquired copy number alterations in adult acute myeloid leukemia genomes. Proc Natl Acad Sci USA 106, 12950-12955 (2009)
3. Susanne Schnittger, Wolfgang Kern, Claudia Tschulik, Tamara Weiss, Frank Dicker, Brunangelo Falini, Claudia Haferlach and Torsten Haferlach: Minimal residual disease levels assessed by NPM1 mutation-specific RQ-PCR provide important prognostic information in AML. Blood 114, 2220-2231 (2009)
4. Lars Bullinger, Konstanze Dohner, Raphael Kranz, Cristoph Stirner, Stefan Frohling, Claudia Scholl, Young Kim, Richard Schlenk, Robert Tibshirani, Hartmut Dohner and Jonathan Pollack: An FLT3 gene-expression signature predicts clinical outcome in normal karyotype AML. Blood 111, 4490-4495 (2008)
5. Susanne Schnittger, Tobias Kohl, Torsten Haferlach, Wolfgang Kern, Wolfgang Hiddemann, Karsten Spiekermann, and Claudia Schoch: KIT-D816 mutations in AML1-ETO-positive AML are associated with impaired event-free and overall survival. Blood 107, 1791-1799 (2006)
6. Claude Preudhomme, Christophe Sagot, Nicolas Boissel, Jean-Michel Cayuela, Isabelle Tigaud, Stéphane de Botton, Xavier Thomas, Emmanuel Raffoux, Charlotte Lamandin, Sylvie Castaigne, Pierre Fenaux, Hervé Dombret and ALFA Group: Favorable prognostic significance of CEBPA mutations in patients with de novo acute myeloid leukemia: A study from the Acute Leukemia French Association (ALFA). Blood 100, 2717-2723 (2002)
7. Rose Padua, Barbara Guinn, Ala Al-Sabah, M. Smith, Christine Taylor, Tom Pettersson, S. Ridge, G. Carter, D White, David Oscier, S. Chevret, and Robert West: RAS, FMS and p53 mutations and poor clinical outcome in myelodysplasias: A 10-year follow-up. Leukemia 12, 887-892 (1998)
8. Anna Pulliam-Leath, Samantha Ciccone, Grzegorz Nalepa, Xiaxin Li, Yue Si, Leticia Miravalle, Danielle Smith, Jin Yuan, Jingling Li, Praveen Anur, Attilio Orazi, Gail Vance, Feng-Chun Yang, Helmut Hanenberg, Grover Bagby and D. Wade Clapp: Genetic disruption of both Fancc and Fancg in mice recapitulates the hematopoietic manifestations of Fanconi anemia. Blood (2010) (Epub ahead of print)
9. June Li, Daniel Sejas, Xiaoling Zhang, Yuhui Qiu, Kalpana Nattamai, Reena Rani, Keaney Rathbun, Hartmut Geiger, David Williams, Grover Bagby, and Qishen Pang: TNF-alpha induces leukemic clonal evolution ex vivo in Fanconi anemia group C murine stem cells. J Clin Invest 117, 3283-3295 (2007)
10. Grover Bagby: Discovering early molecular determinants of leukemogenesis. J Clin Invest 118, 847-850 (2008)
11. Fulu Liu, Ghada Kunter, Maxwell Krem, William Eades, Jennifer Cain, Michael Tomasson, Lothar Hennighausen and Daniel Link: Csf3r mutations in mice confer a strong clonal HSC advantage via activation of Stat5. J Clin Invest 118, 946-955 (2008)
12. M. William Lensch, R. Keaney Rathbun, Susan Olson, Gary Jones and Grover Bagby Jr: Selective pressure as an essential force in molecular evolution of myeloid leukemic clones: A view from the window of Fanconi anemia. Leukemia 13, 1784-1789 (1999)
13. Brian Druker, François Guilhot, Stephen O'Brien, Insa Gathmann, Hagop Kantarjian, Norbert Gattermann, Michael Deininger, Richard Silver, John Goldman, Richard Stone, Francisco Cervantes, Andreas Hochhaus, Bayard Powell, Janice Gabrilove, Philippe Rousselot, Josy Reiffers, Jan Cornelissen, Timothy Hughes, Hermine Agis, Thomas Fischer, Gregor Verhoef, John Shepherd, Giuseppe Saglio, Alois Gratwohl, Johan Nielsen, Jerald Radich, Bengt Simonsson, Kerry Taylor, Michele Baccarani, Charlene So, Laurie Letvak, and Richard Larson for the IRIS Investigators: Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N Engl J Med 355, 2408-2417 (2006)
14. Brian Druker: Translation of the Philadelphia chromosome into therapy for CML. Blood 112, 4808-4817 (2008)
15. Jeffrey Tyner, Michael Deininger, Marc Loriaux, Bill Chang, Jason Gotlib, Stephanie Willis, Heidi Erickson, Tibor Kovacsovics, Thomas O'Hare, Michael Heinrich and Brian Druker: RNAi screen for rapid therapeutic target identification in leukemia patients. Proc Natl Acad Sci USA 106, 8695-8700 (2009)
16. Sheri Tinnell Dorsam, Christina Ferrell, Glenn Dorsam, Mika Kakefuda Derynck, Ulka Vijapurkar, Daniel Khodabakhsh, Bonnie Pau, Hillary Bernstein, Christopher Haqq, Corey Largman, and H. Jeffrey Lawrence: The transcriptome of the leukemogenic homeoprotein HOXA9 in human hematopoietic cells. Blood 103, 1676-1684 (2004)
17. Christian Bach, Sebastian Buhl, Dorothée Mueller, María-Paz García-Cuéllar, Emanuel Maethner, and Robert Slany: Leukemogenic transformation by HOXA cluster genes. Blood 115, 2910-2918 (2010)
18. Carolina Abramovich and R. Keith Humphries: Hox regulation of normal and leukemic hematopoietic stem cells. Curr Opin Hematol 12, 210-216 (2005)
19. Unnur Thorsteinsdottir, Aline Mamo, Evert Kroon, Lori Jerome, Janet Bijl, H. Jeffrey Lawrence, Keith Humphries and Guy Sauvageau: Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 99, 121-129 (2002)
20. Evert Kroon, Jana Krosl, Unnur Thorsteinsdottir, Soheyl Baban, Arthur Buchberg and Guy Sauvageau: Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J 17, 3714-3725 (1998)
21. Paul Ayton and Michael Cleary: Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 17, 2298-2307 (2003)
22. Michael Milsom, Bernhard Schiedlmeier, Jeff Bailey, Mi-Ok Kim, Dandan Li, Michael Jansen, Abdullah Mahmood Ali, Michelle Kirby, Christopher Baum, Leslie Fairbairn and David Williams: Ectopic HOXB4 overcomes the inhibitory effect of tumor necrosis factor-alpha on Fanconi anemia hematopoietic stem and progenitor cells. Blood 113, 5111-5120 (2009)
23. Joseph Wiemels, Zhijian Xiao, Patricia Buffler, Ana Maia, Xiaomei Ma, Brian Dicks, Martyn Smith, Luoping Zhang, James Feusner, John Wiencke, Kathy Pritchard- Jones, Helena Kempski, and Mel Greaves: In utero origin of t(8;21) AML1-ETO translocations in childhood acute myeloid leukemia. Blood 99, 3801-3805 (2002)
24. Hiroshi Mori, Susan Colman, Zhijian Xiao, Anthony Ford, Lyn Healy, Craig Donaldson, Jill Hows, Cristina Navarrete and Mel Greaves: Chromosome translocations and covert leukemic clones are generated during normal fetal development. Proc Natl Acad Sci USA 99, 8242-8247 (2002)
25. Dengli Hong, Rajeev Gupta, Philip Ancliff, Ann Atzberger, John Brown, Shamit Soneji, Joanne Green, Sue Colman, Wanda Piacibello, Veronica Buckle, Shinobu Tsuzuki, Mel Greaves and Tariq Enver: Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science 319, 336-339 (2008)
26. Robert Unckless and H. Allen Orr, The population genetics of adaptation: multiple substitutions on a smooth fitness landscape. Genetics 183, 1079-1086 (2009)
27. Grover Bagby and Gabrielle Meyers: Myelodysplasia and acute leukemia as late complications of marrow failure: future prospects for leukemia prevention. Hematol Oncol Clin North Am 23, 361-376 (2009)
28. Peter Lakatos and Lazlo Lakatos: Risk for colorectal cancer in ulcerative colitis: changes, causes and management strategies. World J Gastroenterol 14, 3937-3947 (2008)
29. Robert Hammer, James Richardson, William Simmons, A. L. White, Maxime Breban, and Joel Taurog: High prevalence of colorectal cancer in HLA-B27 transgenic F344 rats with chronic inflammatory bowel disease. J Investig Med 43, 262-268 (1995)
30. Uwe Rudolph, Milton Finegold, Susan Rich, Gregory Harriman, Yogambal Srinivasan, Philippe Brabet, Guylain Boulay, Allan Bradley and Lutz Birnbaumer: Ulcerative colitis and adenocarcinoma of the colon in G alpha i2- deficient mice. Nat Genet 10, 143-150 (1995)
31. Boryana Popivanova, Kazuya Kitamura, Yu Wu, Toshikazu Kondo, Takashi Kagaya, Shiuchi Kaneko, Masanobu Oshima, Chifumi Fujii and Naofumi Mukaida: Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis. J Clin Invest 118, 560-570 (2008)
32. Yoshitaka Kamegaya, Yiochi Hiasa, Lawrence Zukerberg, Nina Fowler, Jason Blackard, Wenyu Lin, Won Choe, Emmett Schmidt and Raymond Chung: Hepatitis C virus acts as a tumor accelerator by blocking apoptosis in a mouse model of hepatocarcinogenesis. Hepatology 41, 660-667 (2005)
33. Heike Bantel and Klaus Schulze-Osthoff: Apoptosis in hepatitis C virus infection. Cell Death Differ 10, S48-S58 (2003)
34. Katerina Dvorakova, Claire Payne, Lois Ramsey, Harris Bernstein, Hana Holubec, Melissa Chavarria, Carol Bernstein, Richard Sampliner, Catherine Riley, Anil Prasad and Harinder Garewal: Apoptosis resistance in Barrett's esophagus: Ex vivo bioassay of live stressed tissues. American Journal of Gastroenterology 100, 424-431 (2005)
35. Tohru Niwa, Tetsuya Tsukamoto, Takeshi Toyoda, Akiko Mori, Harunari Tanaka, Takao Maekita, Masao Ichinose, Masae Tatematsu and Toshikazu Ushijima: Inflammatory Processes Triggered by Helicobacter pylori Infection Cause Aberrant DNA Methylation in Gastric Epithelial Cells. Cancer Res 70, 1430-1440 (2010)
36. Alberto Mantovani: Cancer: Inflaming metastasis. Nature 457, 36-37 (2009)
37. Omar Sharif, Viacheslav Bolshakov, Stephanie Raines, Peter Newham and Neil Perkin: Transcriptional profiling of the LPS induced NF-kappaB response in macrophages. BMC Immunol 8, 1 (2007)
38. Florian Greten, Lars Eckmann, Tim Greten, Jin Mo Park, Zhi-Wei Li, Laurence Egan, Martin Kagnoff and Michael Karin: IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118, 285-296 (2004)
39. Jun-Li Luo, Shin Maeda, Li-Chung Hsu, Hideo Yagita and Michael Karin: Inhibition of NF-kappaB in cancer cells converts inflammation- induced tumor growth mediated by TNFalpha to TRAIL-mediated tumor regression. Cancer Cell 6, 297-305 (2004)
40. James Klaunig, Yong Xu, Jason Isenberg, Stephen Bachowski, Kyle Kolaja, Jiazhong Jiang, Donald Stevenson and Earl Walborg: The role of oxidative stress in chemical carcinogenesis. Environ Health Perspect 106, 289-295 (1998)
41. Scott Maynard, Shepherd Schurman, Charlotte Harboe, Nadja de Souza-Pinto and Vilhelm Bohr: Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30, 2-10 (2009).
42. Kaori Ishikawa, Keizo Takenaga, Miho Akimoto, Nobuko Koshikawa, Aya Yamaguchi, Hirotake Imanishi, Kazuto Nakada, Yoshio Honma, Jun-Ichi Hayashi: ROSgenerating mitochondrial DNA mutations can regulate tumor cell metastasis. Science 320, 661-664 (2008).
43. M. A. Joyce, K. A. Walters, S. E. Lamb, M. M. Yeh, L. F. Zhu, N. Kneteman, J. S. Doyle, M. G. Katze and D. L. Tyrrell, HCV induces oxidative and ER stress, and sensitizes infected cells to apoptosis in SCID/Alb-uPA mice. PLoS Pathog 5, e1000291 (2009).
44. Jakob Seidelin and Ole Nielsen: Attenuated apoptosis response to Fas-ligand in active ulcerative colitis. Inflamm Bowel Dis 14, 1623-1629 (2008)
45. H. Allen Orr: The population genetics of beneficial mutations. Philos Trans R Soc Lond B Biol Sci 365, 1195- 1201 (2010)
46. Michael Nachman, Hopi Hoekstra and Susan D'Agostino: The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA 100, 5268-5273 (2003)
47. Michael Majerus and Nicholas Mundy: Mammalian melanism: natural selection in black and white. Trends Genet 19, 585-588 (2003)
48. H. Allen Orr: Fitness and its role in evolutionary genetics. Nat Rev Genet 10, 531-539 (2009)
49. Ivana Bjedov, Olivier Tenaillon, Bénédicte Gérard,Valeria Souza, Erick Denamur, Miroslav Radman, François Taddei and Ivan Matic: Stress-induced mutagenesis in bacteria. Science 300, 1404-1409 (2003).
50. Patricia Foster, Stress responses and genetic variation in bacteria. Mutat Res 569, 3-11 (2005).
51. Alexander Anderson, AlissaWeaver, Peter Cummings and Vito Quaranta: Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127, 905-915 (2006)
52. Neal Young, Rodrigo Calado and Phillip Scheinberg: Current concepts in the pathophysiology and treatment of aplastic anemia. Blood 108, 2509-2519 (2006)
53. Antonio Risitano, Jaroslaw Maciejewski, Spencer Green, Magdalena Plasilova, Weihua Zeng and Neal Young: In-vivo dominant immune responses in aplastic anaemia: molecular tracking of putatively pathogenetic T-cell clones by TCR beta-CDR3 sequencing. LANCET 364, 355-364 (2004)
54. Elaine Sloand, Sonnie Kim, Jaroslaw Maciejewski, John Tisdale, Dean Follmann, and Neal Young: Intracellular interferon-gamma in circulating and marrow T cells detected by flow cytometry and the response to immunosuppressive therapy in patients with aplastic anemia. Blood 100, 1185-1191 (2002)
55. Michael Bloom, Adam Wolk, Karen Simon-Stoos, Julie Bard, Jichun Chen and Neal Young: A mouse model of lymphocyte infusion-induced bone marrow failure. Exp Hematol 32, 1163-1172 (2004).
56. Weihua Zeng, Sachiko Kajigaya, Guibin Chen, Antonio Risitano, Olga Nunez and Neal Young: Transcript profile of CD4+ and CD8+ T cells from the bone marrow of acquired aplastic anemia patients. Exp Hematol 32, 806-814 (2004)
57. Weihua Zeng, Guibin Chen, Sachiko Kajigaya, Olga Nunez, Alexandra Charrow, Eric Billings and Neal Young: Gene expression profiling in CD34 cells to identify differences between aplastic anemia patients and healthy volunteers. Blood 103, 325-332 (2004)
58. Johan de Winter and Hans Joenje: The genetic and molecular basis of Fanconi anemia. Mutat Res 668, 11-19 (2009)
59. Grover Bagby and Blanche Alter: Fanconi anemia. Semin Hematol 43, 147-156 (2006
60. Grover Bagby: Genetic basis of Fanconi anemia. Curr Opin Hematol 10, 68-76 (2003)
61. Fiona Vaz, Helmut Hanenberg, Beatrice Schuster, Karen Barker, Constanze Wiek, Verena Erven, Kornelia Neveling, Daniela Endt, Ian Kesterton, Flavia Autore, Franca Fraternali, Marcel Freund, Linda Hartmann, David Grimwade, Roland Roberts, Heiner Schaal, Shehla Mohammed, Nazneen Rahman, Detlev Schindler and Christopher Mathew: Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat Genet 42, 406-409 (2010)
62. Arleen Auerbach, Barbara Adler and R. S. Chaganti: Prenatal and postnatal diagnosis and carrier detection of Fanconi anemia by a cytogenetic method. Pediatrics 67, 128-135 (1981)
63. Guido Fanconi: Familiare infantile perniziosaartige anaemia (pernizioses blutbild und konstitution). Jahrb Kinderhilkd 117, 257-280 (1927)
64. Grover Bagby and Gabrielle Meyers: Bone Marrow Failure as a Risk Factor for Clonal Evolution: Prospects for Leukemia Prevention. Hematology 2007, 40-46 (2007)
65. Phillip Rosenberg, Mark Greene and Blanche Alter, Cancer incidence in persons with Fanconi anemia. Blood 101, 822-826 (2003)
66. Qishen Pang, Tracy Christianson, Winifred Keeble, Jane Diaz, Gregory Faulkner, Carol Reifsteck, Susan Olson, and Grover Bagby: The Fanconi anemia complementation group C gene product: structural evidence of multifunctionality. Blood 98, 1392-1401 (2001)
67. Laura Hays, Winifred Keeble, Jane Yates, R. Keaney Rathbun, Tara Koretsky, Susan Olson, Zejin Sun, D. Wade Clapp, and Grover Bagby: Human FANCC is hypomorphic in murine Fancc-deficient cells. Blood (2010)(Epub ahead of print)
68. Carlo Dufour, Anna Corcione, Johanna Svahn, Riccardo Haupt, Nicoletta Battilana, and Vito Pistoia: Interferon gamma and tumour necrosis factor alpha are overexpressed in bone marrow T lymphocytes from paediatric patients with aplastic anaemia. Br J Haematol 115, 1023-1031 (2001)
69. Carlo Dufour, Anna Corcione, Johanna Svahn, Riccardo Haupt, Vincenzo Poggi, Albert Nandor Béka'ssy, Rosanna Scimè, Angela Pistorio, and Vito Pistoia: TNF-? and IFN-? are over expressed in the bone marrow of Fanconi anemia patients and TNF-? suppresses erythropoiesis in vitro. Blood 102, 2053-2059 (2003)
70. Scott Vanderwerf, Johanna Svahn, Susan Olson, R. Keaney Rathbun, Christina Harrington, Jane Yates, Winifred Keeble, David Anderson, Praveen Anur, Noemi Pereira, Daniela Pilonetto, Ricardo Pasquini, and Grover Bagby: TLR8-dependent TNF? overexpression in Fanconi anemia group C cells. Blood 114, 5290-5298 (2009)
71. Qishen Pang, Winifred Keeble, Tracy Christianson, Gregory Faulkner, and Grover Bagby: FANCC interacts with hsp70 to protect hematopoietic cells from IFN?/TNF?- mediated cytotoxicity. EMBO J 20, 4478-4489 (2001)
72. Paul Koh, Grant Hughes, Gregory Faulkner, Winifred Keeble and Grover Bagby: The Fanconi anemia group C gene product modulates apoptotic responses to tumor necrosis factor-a and Fas ligand but does not suppress expression of receptors of the tumor necrosis factor receptor superfamily. Exp Hematol 27, 1-8 (1999)
73. Michael Whitney, Gordon Royle, Michelle Low, Michelle Kelly, Michael Axthelm, Carol Reifsteck, Susan Olson, Robert Braun, Michael Heinrich, R. Keaney Rathbun, Grover Bagby and Markus Grompe: Germ cell defects and hematopoietic hypersensitivity to g-interferon in mice with a targeted disruption of the Fanconi anemia C gene. Blood 88, 49-58 (1996)
74. Laura Haneline, Hal Broxmeyer, Scott Cooper, Giao Hangoc, Madeleine Carreau, Manuel Buchwald and D. Wade Clapp: Multiple inhibitory cytokines induce deregulated progenitor growth and apoptosis in hematopoietic cells from FAC-/- mice. Blood 91, 4092-4098 (1998)
75. Simona Pigullo1, Elisa Ferretti2, Marina Lanciotti, Maurizio Bruschi, Giovanni Candiano, Johanna Svahn, Laura Haneline, Carlo Dufour, Vito Pistoia, Anna Corcione: Human Fanconi A cells are susceptible to TRAIL-induced apoptosis. Br J Haematol 136, 315-318 (2007)
76. Yue Si, Samantha Ciccone, Feng-Chun Yang, Jin Yuan, Daisy Zeng, Shi Chen, Henri van de Vrugt, John Critser, Fre Arwert, Laura Haneline, and D. Wade Clapp: Continuous in vivo infusion of interferon-gamma enhances engraftment of syngeneic wild-type cells in Fanca-/- and Fancg-/- mice. Blood 108, 4283-4287 (2006)
77. Xiaxin Li, Yanzhu Yang, Jin Yuan, Ping Hong, Brian Freie, Attilio Orazi, Laura Haneline, and D. Wade Clapp: Continuous in vivo infusion of interferon-gamma (IFN-?) preferentially reduces myeloid progenitor numbers and enhances engraftment of syngeneic wildtype cells in Fancc- /- mice. Blood 104, 1209 (2004)
78. Daniel Sejas, Reena Rani, Yuhui Qiu, Xiaoling Zhang, Sara Fagerlie, Hiroyasu Nakano, David Williams, and Qishen Pang: Inflammatory reactive oxygen speciesmediated hemopoietic suppression in Fancc-deficient mice. J Immunol 178, 5277-5287 (2007)
79. Xiaoling Zhang, Daniel Sejas,Yuhui Qiu, David Williams, and Qishen Pang: Inflammatory ROS promote and cooperate with the Fanconi anemia mutation for hematopoietic senescence. J Cell Sci 120, 1572-1583 (2007)
80. Qishen Pang, Winifred Keeble, Jane Diaz, Tracy Christianson, Sara Fagerlie, Keaney Rathbun, Gregory Faulkner, Michael O'Dwyer, and Grover Bagby: Role of double-stranded RNA-dependent protein kinase in mediating hypersensitivity of Fanconi anemia complementation group C cells to interferon gamma, tumor necrosis factor-alpha, and double-stranded RNA. Blood 97, 1644-1652 (2001)
81. R. Keaney Rathbun, Tracy Christianson, Gregory Faulkner, Gary Jones, Winifred Keeble, Michael O'Dwyer, and Grover Bagby: Interferon-g-induced apoptotic responses of Fanconi anemia group C hematopoietic progenitor cells involve caspase 8-dependent activation of caspase 3 family members. Blood 96, 4204-4211 (2000)
82. Xiaoling Zhang, June Li, Daniel Sejas, Keaney Rathbun, Grover Bagby, and Qishen Pang: The Fanconi anemia proteins functionally interact with the protein kinase regulated by RNA (PKR). J Biol Chem 279, 43910-43919 (2004)
83. Khadijeh Bijangi-Vishehsaraei, M. Reza Saadatzadeh, Adam Werne, Kristina Wilson McKenzie, Reuben Kapur, Hidenori Ichijo, and Laura Haneline: Enhanced TNF-?-induced apoptosis in Fanconi anemia type C-deficient cells is dependent on apoptosis signalregulating kinase. Blood 106, 4124-4130 (2005)
84. Qishen Pang, Tracy Christianson, Winifred Keeble, Tara Koretsky and Grover Bagby: The anti-apoptotic function of Hsp70 in the interferon-inducible doublestranded RNA-dependent protein kinase-mediated death signaling pathway requires the Fanconi anemia protein, FANCC. Journal of Biological Chemistry 277, 49638-49643 (2002)
85. John Schultz and Nasrollah Shahidi: Tumor necrosis factor-alpha overproduction in Fanconi's anemia. Am J Hematol 42, 196-201 (1993)
86. Asmin Tulpule, M. William Lensch, Justine Miller, Karyn Austin, Alan D'Andrea, Thorsten M. Schlaeger, Akiko Shimamura, and George Q. Daley: Knockdown of Fanconi anemia genes in human embryonic stem cells reveals early developmental defects in the hematopoietic lineage. Blood 115, 3453-3462 (2010)
87. Eva Guinan: Acquired aplastic anemia in childhood. Hematol Oncol Clin North Am 23, 171-191 (2009)
88. Yigal Dror and Melvin Freedman: Shwachman- Diamond syndrome marrow cells show abnormally increased apoptosis mediated through the Fas pathway. Blood 97, 3011-3016 (2001)
89. Inga Köllner, Beate Sodeik, Sabine Schreek, Holger Heyn,Nils von Neuhoff, Manuela Germeshausen, Cornelia Zeidler, Martin Krüger, Brigitte Schlegelberger, Karl Welte, and Carmela Beger: Mutations in neutrophil elastase causing congenital neutropenia lead to cytoplasmic protein accumulation and induction of the unfolded protein response. Blood 108, 493-500 (2006)
90. Andrew Yoon, Guang Peng, Yves Brandenburg, Ornella Zollo, Wei Xu, Eduardo Rego, and Davide Ruggero: Impaired control of IRES-mediated translation in X-linked dyskeratosis congenita. Science 312, 902-906 (2006)
91. Michaela Gross, Helmut Hanenberg, Stephan Lobitz, Richard Friedl, Sabine Herterich, Ralf Dietrich, Bernd Gruhn, Detlev Schindler and Holger Hoehn: Reverse mosaicism in Fanconi anemia: natural gene therapy via molecular self-correction. Cytogenet Cell Genet 98, 126-135 (2002)
92. John Gregory, Jr. , John Wagner, Peter Verlander, Orna Levran, Sat Dev Batish, Cindy Eide, Amy Steffenhagen, Betsy Hirsch, Arleen Auerbach: Somatic mosaicism in Fanconi anemia: evidence of genotypic reversion in lymphohematopoietic stem cells. Proc Natl Acad Sci USA 98, 2532-2537 (2001)
93. Quinten Waisfisz, Neil Morgan, Maria Savino, Johan de Winter, Carola van Berkel, Maureen Hoatlin, Leonarda Ianzano, Rachel Gibson, Fre Arwert, Anna Savoia, Christopher Mathew, Jan Pronk, and Hans Joenje: Spontaneous functional correction of homozygous Fanconi anaemia alleles reveals novel mechanistic basis for reverse mosaicism. Nat Genet 22, 379-383 (1999)
94. Anuj Mankad, Toshiyasu Taniguchi, Barbara Cox, Yassmine Akkari, R. Keaney Rathbun, Lora Lucas, Grover Bagby, Susan Olson, Alan D'Andrea, and Markus Grompe: Natural gene therapy in monozygotic twins with Fanconi anemia. Blood 107, 3084-3090 (2006)
95. Brian Freie, Xiaxin Li, Samantha Ciccone, Kathy Nawa, Scott Cooper, Catherine Vogelweid, Laurel Schantz, Laura Haneline, Attilio Orazi, Hal Broxmeyer, Suk-Hee Lee, and D. Wade Clapp: Fanconi anemia type C and p53 cooperate in apoptosis and tumorigenesis. Blood 102, 4146-4152 (2003)
96. Xiaxin Li, Michelle Le Beau, Samantha Ciccone, Feng- Chun Yang, Brian Freie, Shi Chen, Jin Yuan, Ping Hong,Attilio Orazi, Laura Haneline, and D. Wade Clapp: Ex vivo culture of Fancc-/- stem/progenitor cells predisposes cells to undergo apoptosis, and surviving stem/progenitor cells display cytogenetic abnormalities and an increased risk of malignancy. Blood 105, 3465-3471 (2005)
97. Laura Haneline, Xiaxin Li, Samantha Ciccone, Ping Hong, Yanzhu Yang, Hal Broxmeyer, Suk-Hee Lee, Attilio Orazi, Edward Srour, and D. Wade Clapp: Retroviralmediated expression of recombinant Fancc enhances the repopulating ability of Fancc-/- hematopoietic stem cells and decreases the risk of clonal evolution. Blood 101, 1299-1307 (2003)
98. Pachiyappan Kamarajan, Nian-Kang Sun and Chuck C.-K. Chao: Up-regulation of FLIP in cisplatin-selected HeLa cells causes cross-resistance to CD95/Fas death signalling. Biochem J 376, 253-260 (2003)
99. Shenghao Jin, Huiwu Zhao, Yan Yi, Yuji Nakata, Anna Kalota, and Alan Gewirtz: c-Myb binds MLL through menin in human leukemia cells and is an important driver of MLL-associated leukemogenesis. J Clin Invest 120, 593- 606 (2010)
100. Francesco Fazi, Serena Racanicchi, Giuseppe Zardo, Linda Starnes, Marco Mancini, Lorena Travaglini, Daniela Diverio, Emanuele Ammatuna, Giuseppe Cimino,Francesco Lo-Coco, Francesco Grignani, and Clara Nervi: Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein. Cancer Cell 12, 457-466 (2007)
101. Paul Ayton, Everett Chen, and Michael Cleary: Binding to nonmethylated CpG DNA is essential for target recognition, transactivation, and myeloid transformation by an MLL oncoprotein. Mol Cell Biol 24, 10470-10478 (2004)
102. Maria Figueroa, Bas Wouters, Lucy Skrabanek, Jacob Glass, Yushan Li, Claudia Erpelinck-Verschueren, Anton Langerak, Bob Löwenberg, Melissa Fazzari, John Greally, Peter Valk, Ari Melnick, and Ruud Delwel: Genome-wide epigenetic analysis delineates a biologically distinct immature acute leukemia with myeloid/T-lymphoid features. Blood 113, 2795-2804 (2009)
103. Ting Xi Liu, Michael Becker, Jaroslav Jelinek, Wen- Shu Wu, Min Deng, Natallia Mikhalkevich, Karl Hsu, Clara Bloomfield, Richard Stone, Daniel DeAngelo, Ilene Galinsky, Jean-Pierre Issa, Michael Clarke, and A Thomas Look: Chromosome 5q deletion and epigenetic suppression of the gene encoding alpha-catenin (CTNNA1) in myeloid cell transformation. Nat Med 13, 78-83 (2007)
104. Joanna Baxter, Linda M Scott, Peter J Campbell, Clare East, Nasios Fourouclas, Soheila Swanton, George S Vassiliou, Anthony J Bench, Elaine M Boyd, Natasha Curti, Mike A Scott, Wendy N Erber, and Anthony R Green, Acquired mutation of the tyrosine kinase JAK2 in human myeloproliferative disorders. LANCET 365, 1054-1061 (2005)
105. Chloé James, Valérie Ugo, Jean-Pierre Le Couédic, Judith Staerk, François Delhommeau, Catherine Lacout, Loïc Garçon, Hana Raslova, Roland Berger, Annelise Bennaceur-Griscelli, Jean Luc Villeval, Stefan Constantinescu, Nicole Casadevall, and William Vainchenker: A unique clonal JAK2 mutation leading to constitutive signalling causes polycythaemia vera. Nature 434, 1144-1148 (2005)
106. Robert Kralovics, Francesco Passamonti, Andreas Buser, Soon-Siong Teo, Ralph Tiedt, Jakob Passweg, Andre Tichelli, Mario Cazzola, and Radek Skoda: A gainof- function mutation of JAK2 in myeloproliferative disorders. N Engl J Med 352, 1779-1790 (2005)
107. Ross Levine, Martha Wadleigh, Jan Cools, Benjamin Ebert, Gerlinde Wernig, Brian Huntly, Titus Boggon, Iwona Wlodarska, Jennifer Clark, Sandra Moore, Jennifer Adelsperger, Sumin Koo, Jeffrey Lee, Stacey Gabriel, Thomas Mercher, Alan D?Andrea, Stefan Fröhling, Konstanze Döhner, Peter Marynen, Peter Vandenberghe, Ruben Mesa, Ayalew Tefferi, James Griffin, Michael Eck, William Sellers, Matthew Meyerson, Todd Golub, Stephanie Lee, and D. Gary Gilliland: Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia, and myeloid metaplasia with myelofibrosis. Cancer Cell 7, 387-397 (2005)
108. Runxiang Zhao, Shu Xing, Zhe Li, Xueqi Fu, Qingshan Li, Sanford Krantz, and Zhizhuang Joe Zhao: Identification of an acquired JAK2 mutation in polycythemia vera. J Biol Chem 280, 22788-22792 (2005)
109. Catriona Jamieson, Jason Gotlib, Jeffrey Durocher, Mark Chao, M. Rajan Mariappan, Marla Lay, Carol Jones, James Zehnder , Stan Lilleberg, and Irving Weissman: The JAK2 V617F mutation occurs in hematopoietic stem cells in polycythemia vera and predisposes toward erythroid differentiation. Proc Natl Acad Sci USA 103, 6224-6229 (2006)
110. Thomas Bumm, Collin Elsea, Amie Corbin, Marc Loriaux, Daniel Sherbenou, Lisa Wood, Jutta Deininger, Richard Silver, Brian Druker, and Michael Deininger: Characterization of murine JAK2V617Fpositive myeloproliferative disease. Cancer Res 66, 11156-11165 (2006)
111. Catherine Lacout, Didier Pisani, Micheline Tulliez, Françoise Moreau Gachelin, William Vainchenker, and Jean-Luc Villeval: JAK2V617F expression in murine hematopoietic cells leads to MPD mimicking human PV with secondary myelofibrosis. Blood 108, 1652-1660 (2006)
112. Gerlinde Wernig, Thomas Mercher, Rachel Okabe, Ross Levine, Benjamin Lee, and D. Gary Gilliland: Expression of Jak2V617F causes a polycythemia vera-like disease with associated myelofibrosis in a murine bone marrow transplant model. Blood 107, 4274-4281 (2006)
113. Ralph Tiedt, Hui Hao-Shen, Marta Sobas, Renate Looser, Stephan Dirnhofer, Jürg Schwaller, and Radek Skoda: Ratio of mutant JAK2-V617F to wild-type Jak2 determines the MPD phenotypes in transgenic mice. Blood 111, 3931-3940 (2008)
114. Hajime Akada, Dongqing Yan, Haiying Zou, Steven Fiering, Robert Hutchison, and M. Golam Mohi: Conditional expression of heterozygous or homozygous Jak2V617F from its endogenous promoter induces a polycythemia vera-like disease. Blood 115, 3589-3597 (2010)
115. Juan Li, Dominik Spensberger, Jong Sook Ahn, Shubha Anand, Philip Beer, Cedric Ghevaert, Edwin Chen, Ariel Forrai, Linda Scott, Rita Ferreira, Peter Campbell, Steve Watson, Pentao Liu, Wendy Erber, Brian Huntly, Katrin Ottersbach, and Anthony Green: JAK2 conditional knock-in mouse model of JAK2 V617Fpositive essential thrombocythemia. Blood (2010) (Epub ahead of print)
116. Ann Mullally, Steven Lane, Brian Ball, Christine Megerdichian, Rachel Okabe, Fatima Al-Shahrour, Mahnaz Paktinat, J. Erika Haydu, Elizabeth Housman, Allegra Lord, Gerlinde Wernig, Michael Kharas, Thomas Mercher, Jeffery Kutok, D. Gary Gilliland, and Benjamin Ebert: Physiological Jak2V617F expression causes a lethal myeloproliferative neoplasm with differential effects on hematopoietic stem and progenitor cells. Cancer Cell 17, 584-596 (2010)
117. Kalindi Parmar, Alan D?Andrea, and Laura Niedernhofer: Mouse models of Fanconi anemia. Mutat Res 668, 133-140 (2009)
118. Ming Zhang, Jun Qian, Xianying Xing, Feng-Ming Kong, Lujun Zhao, Ming Chenand Theodore Lawrence: Inhibition of the tumor necrosis factor-alpha pathway is radioprotective for the lung. Clin Cancer Res 14, 1868-1876 (2008)
119. Elisa Rumi: Familial chronic myeloproliferative disorders: The state of the art. Hematol Oncol 26, 131-138 (2008)
120. Outi Kilpivaara, Semanti Mukherjee, Alison Schram, Martha Wadleigh, Ann Mullally, Benjamin Ebert, Adam Bass, Sachie Marubayashi, Adriana Heguy, Guillermo Garcia-Manero, Hagop Kantarjian, Kenneth Offit, Richard Stone, D Gary Gilliland, Robert Klein, and Ross Levine: A germline JAK2 SNP is associated with predisposition to the development of JAK2(V617F)-positive myeloproliferative neoplasms. Nat Genet 41, 455-459 (2009)
121. Damla Olcaydu, Ashot Harutyunyan, Roland Jäger, Tiina Berg, Bettina Gisslinger, Ingrid Pabinger, Heinz Gisslinger, and Robert Kralovics: A common JAK2 haplotype confers susceptibility to myeloproliferative neoplasms. Nat Genet 41, 450-454 (2009)
122. Amy Jones, Andrew Chase, Richard Silver, David Oscier, Katerina Zoi, Y Lynn Wang, Holger Cario, Heike Pahl, Andrew Collins, Andreas Reite, Francis Grand, and Nicholas Cross: JAK2 haplotype is a major risk factor for the development of myeloproliferative neoplasms. Nat Genet 41, 446-449 (2009)
123. Dean Felsher: Tumor dormancy and oncogene addiction. APMIS 116, 629-637 (2008)
124. Jos Jonkers and Anton Berns: Oncogene addiction: sometimes a temporary slavery. Cancer Cell 6, 535-538 (2004)
125. Paul Workman: Cancer genome targets: RAF-ing up tumor cells to overcome oncogene addiction. Expert Rev Anticancer Ther 2, 611-614 (2002)
126. Jennifer Clark, Jan Cools, David Curley, Jin-Chen Yu, Nathalie Lokker, Neill A. Giese, and D. Gary Gilliland: Variable sensitivity of FLT3 activation loop mutations to the small molecule tyrosine kinase inhibitor MLN518. Blood 104, 2867-2872 (2004)
127. Ellen Weisberg, Christina Boulton, Louise Kelly, Paul Manley, Doriano Fabbro, Thomas Meyer, D. Gary Gilliland, and James Griffin: Inhibition of mutant FLT3 receptors in leukemia cells by the small molecule tyrosine kinase inhibitor PKC412. Cancer Cell 1, 433-443 (2002)
128. Stefan Fröhling, Claudia Scholl, Ross Levine, Marc Loriaux, Titus Boggon, Olivier Bernard, Roland Berger, Hartmut Döhner, Konstanze Döhner, Benjamin Ebert, Sewit Teckie, Todd Golub, Jingrui Jiang, Marcus Schittenhelm, Benjamin Lee, James Griffin, Richard Stone, Michael Heinrich, Michael Deininger, Brian Druker, and D. Gary Gilliland: Identification of driver and passenger mutations of FLT3 by high-throughput DNA sequence analysis and functional assessment of candidate alleles. Cancer Cell 12, 501-513 (2007)
129. Paul Wan, Mathew Garnett, S. Mark Roe, Sharlene Lee, Dan Niculescu-Duvaz, Valerie Good, C. Michael Jones, Christopher Marshall, Caroline Springer, David Barford, and Richard Marais: Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell 116, 855-867 (2004)