Drosophila melanogaster: a model and a tool to investigate malignancy and identify new therapeutics

For decades, lower-model organisms such as Drosophila melanogaster have often provided the first glimpse into the mechanism of action of human cancer-related proteins, thus making a substantial contribution to elucidating the molecular basis of the disease. More recently, D. melanogaster strains that are engineered to recapitulate key aspects of specific types of human cancer have been paving the way for the future role of this 'workhorse' of biomedical research, helping to further investigate the process of malignancy, and serving as platforms for therapeutic drug discovery.

[1]  Noemi Andor,et al.  Asymmetry-defective oligodendrocyte progenitors are glioma precursors. , 2011, Cancer cell.

[2]  B. Edgar,et al.  The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration , 2010, Development.

[3]  B. Edgar,et al.  Intestinal stem cell function in Drosophila and mice. , 2012, Current opinion in genetics & development.

[4]  H. Benchabane,et al.  Dual Positive and Negative Regulation of Wingless Signaling by Adenomatous Polyposis Coli , 2008, Science.

[5]  J. Knoblich,et al.  The Par Complex and Integrins Direct Asymmetric Cell Division in Adult Intestinal Stem Cells , 2012, Cell stem cell.

[6]  Neil J Ganem,et al.  DNA breaks and chromosome pulverization from errors in mitosis , 2012, Nature.

[7]  T. Löffler,et al.  A temperature-sensitive brain tumor suppressor mutation of Drosophila melanogaster: Developmental studies and molecular localization of the gene , 1993, Mechanisms of Development.

[8]  B. Purow Notch inhibitors as a new tool in the war on cancer: a pathway to watch. , 2009, Current pharmaceutical biotechnology.

[9]  W. P. Hanratty,et al.  The Drosophila Tumorous lethal hematopoietic oncogene is a dominant mutation in the hopscotch locus , 1993, Molecular and General Genetics MGG.

[10]  Jon R. Armstrong,et al.  A Drosophila Model of Multiple Endocrine Neoplasia Type 2 , 2005, Genetics.

[11]  J. Bolívar,et al.  Epigenetic silencers and Notch collaborate to promote malignant tumours by Rb silencing , 2006, Nature.

[12]  Frank Hirth,et al.  The brain tumor gene negatively regulates neural progenitor cell proliferation in the larval central brain of Drosophila , 2006, Development.

[13]  U. Heberlein,et al.  Aurora-A acts as a tumor suppressor and regulates self-renewal of Drosophila neuroblasts. , 2006, Genes & development.

[14]  O. Sibon,et al.  Contribution of Growth and Cell Cycle Checkpoints to Radiation Survival in Drosophila , 2006, Genetics.

[15]  G. Halder,et al.  A non-cell-autonomous tumor suppressor role for Stat in eliminating oncogenic scribble cells , 2013, Oncogene.

[16]  P. Driscoll,et al.  Anaplastic Lymphoma Kinase Spares Organ Growth during Nutrient Restriction in Drosophila , 2011, Cell.

[17]  G. Kriek,et al.  BOUVARDIN AND DEOXYBOUVARDIN, ANTITUMOR CYCLIC HEXAPEPTIDES FROM BOUVARDIA TERNIFOLIA (RUBIACEAE) , 1978 .

[18]  G. Pelosi,et al.  Alterations of the Notch pathway in lung cancer , 2009, Proceedings of the National Academy of Sciences.

[19]  G. Morata,et al.  Minutes: mutants of drosophila autonomously affecting cell division rate. , 1975, Developmental biology.

[20]  Terry Speed,et al.  Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. , 2007, Genes & development.

[21]  N. Perrimon,et al.  Evidence that stem cells reside in the adult Drosophila midgut epithelium , 2006, Nature.

[22]  Sudhir Kumar,et al.  Comparative Genomics in Eukaryotes , 2005 .

[23]  Tannishtha Reya,et al.  Imaging hematopoietic precursor division in real time. , 2007, Cell stem cell.

[24]  Alexey Khodjakov,et al.  Centrosome Amplification Can Initiate Tumorigenesis in Flies , 2008, Cell.

[25]  S. Hou,et al.  Tumor suppressors Sav/scrib and oncogene ras regulate stem‐cell transformation in adult Drosophila malpighian tubules , 2010, Journal of cellular physiology.

[26]  E. Olson,et al.  A Drosophila model of the rhabdomyosarcoma initiator PAX7-FKHR , 2006, Proceedings of the National Academy of Sciences.

[27]  K. Golic,et al.  Telomere Loss Provokes Multiple Pathways to Apoptosis and Produces Genomic Instability in Drosophila melanogaster , 2008, Genetics.

[28]  H. Richardson,et al.  The Scribble-Dlg-Lgl polarity module in development and cancer: from flies to man. , 2012, Essays in biochemistry.

[29]  G. Morata,et al.  A tumor-suppressing mechanism in Drosophila involving cell competition and the Hippo pathway , 2010, Proceedings of the National Academy of Sciences.

[30]  H. Harris A long view of fashions in cancer research. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[31]  M. Malumbres,et al.  Functional evolution of Polo-like kinases , 2011 .

[32]  C. García-echeverría,et al.  PI3K and mTOR inhibitors: a new generation of targeted anticancer agents. , 2009, Current opinion in cell biology.

[33]  D. Wallace Mitochondria and cancer , 2012, Nature Reviews Cancer.

[34]  William T. Silkworth,et al.  Multipolar Spindle Pole Coalescence Is a Major Source of Kinetochore Mis-Attachment and Chromosome Mis-Segregation in Cancer Cells , 2009, PloS one.

[35]  Ross Cagan,et al.  Drosophila as a novel therapeutic discovery tool for thyroid cancer. , 2010, Thyroid : official journal of the American Thyroid Association.

[36]  Webster K. Cavenee,et al.  A Drosophila Model for EGFR-Ras and PI3K-Dependent Human Glioma , 2009, PLoS genetics.

[37]  G. Halder,et al.  Tumor suppression by cell competition through regulation of the Hippo pathway , 2011, Proceedings of the National Academy of Sciences.

[38]  D. Bilder Epithelial polarity and proliferation control: links from the Drosophila neoplastic tumor suppressors. , 2004, Genes & development.

[39]  M. Scott,et al.  Learning from Jekyll to control Hyde: Hedgehog signaling in development and cancer. , 2010, Trends in molecular medicine.

[40]  Florian Finkernagel,et al.  LINT, a Novel dL(3)mbt-Containing Complex, Represses Malignant Brain Tumour Signature Genes , 2012, PLoS genetics.

[41]  O. Heidenreich,et al.  A Drosophila model identifies calpains as modulators of the human leukemogenic fusion protein AML1-ETO , 2009, Proceedings of the National Academy of Sciences.

[42]  W. Bushman Hedgehog Signaling in Development and Cancer , 2007 .

[43]  Human APC sequesters β-catenin even in the absence of GSK-3β in a Drosophila model , 2008, Oncogene.

[44]  Jun-Yuan Ji,et al.  E2F1 represses β-catenin transcription and is antagonized by both pRB and CDK8 , 2008, Nature.

[45]  Giacomo Cavalli,et al.  Polyhomeotic has a tumor suppressor activity mediated by repression of Notch signaling , 2009, Nature Genetics.

[46]  A. Capobianco,et al.  Notch signalling in solid tumours: a little bit of everything but not all the time , 2011, Nature Reviews Cancer.

[47]  Julia B. Cordero,et al.  Inducible progenitor-derived Wingless regulates adult midgut regeneration in Drosophila , 2012, The EMBO journal.

[48]  R. Dasgupta,et al.  An RNAi-based chemical genetic screen identifies three small-molecule inhibitors of the Wnt/wingless signaling pathway , 2011, Proceedings of the National Academy of Sciences.

[49]  S. Casas-Tintó,et al.  Cell competition time line: winners kill losers, which are extruded and engulfed by hemocytes. , 2012, Cell reports.

[50]  David Bilder,et al.  A tumor suppressive activity of Drosophila Polycomb genes mediated by JAK/STAT signaling , 2009, Nature Genetics.

[51]  T. T. Su,et al.  Chemical genetics and drug screening in Drosophila cancer models. , 2011, Journal of genetics and genomics = Yi chuan xue bao.

[52]  Stephen M. Mount,et al.  The genome sequence of Drosophila melanogaster. , 2000, Science.

[53]  B. Edgar,et al.  EGFR/Ras/MAPK signaling mediates adult midgut epithelial homeostasis and regeneration in Drosophila. , 2011, Cell stem cell.

[54]  M. Bate,et al.  The development of Drosophila melanogaster , 1993 .

[55]  P. A. Hardy,et al.  Reappraisal of the Hansemann—Boveri hypothesis on the origin of tumors , 2005, Cell biology international.

[56]  A. Brand,et al.  Regulating the balance between symmetric and asymmetric stem cell division in the developing brain , 2011, Fly.

[57]  E. Meuillet,et al.  Regulation of the activity of the tumor suppressor PTEN by thioredoxin in Drosophila melanogaster. , 2007, Experimental cell research.

[58]  L. D. Croce,et al.  Roles of the Polycomb group proteins in stem cells and cancer , 2011, Cell Death and Disease.

[59]  J. Krupiński,et al.  Pax genes in embryogenesis and oncogenesis , 2008, Journal of cellular and molecular medicine.

[60]  S. Grewal,et al.  Activated STAT regulates growth and induces competitive interactions independently of Myc, Yorkie, Wingless and ribosome biogenesis , 2012, Development.

[61]  G. Cestra,et al.  A conserved role for the mitochondrial citrate transporter Sea/SLC25A1 in the maintenance of chromosome integrity. , 2009, Human molecular genetics.

[62]  A. Miyawaki,et al.  Elimination of oncogenic neighbors by JNK-mediated engulfment in Drosophila. , 2011, Developmental cell.

[63]  W. Chia,et al.  Polo inhibits progenitor self-renewal and regulates Numb asymmetry by phosphorylating Pon , 2007, Nature.

[64]  H. Richardson,et al.  scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila , 2003, The EMBO journal.

[65]  K. Harvey,et al.  Lgl, aPKC, and Crumbs Regulate the Salvador/Warts/Hippo Pathway through Two Distinct Mechanisms , 2010, Current Biology.

[66]  A. Brand,et al.  Insights into neural stem cell biology from flies , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[67]  C. Gonzalez,et al.  Synergism between altered cortical polarity and the PI3K/TOR pathway in the suppression of tumour growth , 2012, EMBO reports.

[68]  Hyeong-Kyu Lee,et al.  MS‐1020 is a novel small molecule that selectively inhibits JAK3 activity , 2010, British journal of haematology.

[69]  N. Dyson,et al.  Modeling tumor invasion and metastasis in Drosophila , 2011, Disease Models & Mechanisms.

[70]  J. Knoblich,et al.  Mechanisms of Asymmetric Stem Cell Division , 2008, Cell.

[71]  Daniel St Johnston,et al.  A role for Drosophila LKB1 in anterior–posterior axis formation and epithelial polarity , 2003, Nature.

[72]  J. Januschke,et al.  Drosophila asymmetric division, polarity and cancer , 2008, Oncogene.

[73]  T. Schüpbach,et al.  Drosophila brca2 Is Required for Mitotic and Meiotic DNA Repair and Efficient Activation of the Meiotic Recombination Checkpoint , 2008, PLoS genetics.

[74]  J. Downing,et al.  Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. , 2002, Cancer cell.

[75]  A. Ryan,et al.  ZD6474 suppresses oncogenic RET isoforms in a Drosophila model for type 2 multiple endocrine neoplasia syndromes and papillary thyroid carcinoma. , 2005, Cancer research.

[76]  S. Casas-Tintó,et al.  Drosophila SPARC is a self-protective signal expressed by loser cells during cell competition. , 2010, Developmental cell.

[77]  Andrea J. Gerten,et al.  COMPARATIVE VIEW , 2009 .

[78]  C. Sunkel,et al.  Sgt1, a co‐chaperone of Hsp90 stabilizes Polo and is required for centrosome organization , 2009, The EMBO journal.

[79]  D. Glover,et al.  Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles , 1995, Cell.

[80]  H. Muller An analysis of the process of structural change in chromosomes ofDrosophila , 1940, Journal of Genetics.

[81]  D. Raben,et al.  Combinatorial effect of maytansinol and radiation in Drosophila and human cancer cells , 2011, Disease Models & Mechanisms.

[82]  J. C. Pastor-Pareja,et al.  Interaction between RasV12 and scribble clones induces tumour growth and invasion , 2009, Nature.

[83]  Julia B. Cordero,et al.  Oncogenic Ras diverts a host TNF tumor suppressor activity into tumor promoter. , 2010, Developmental cell.

[84]  Tian Xu,et al.  A Genetic Screen in Drosophila for Metastatic Behavior , 2003, Science.

[85]  M. Gatti,et al.  Terminin: A protein complex that mediates epigenetic maintenance of Drosophila telomeres , 2011, Nucleus.

[86]  R. Baumgartner,et al.  Drosophila Pez Acts in Hippo Signaling to Restrict Intestinal Stem Cell Proliferation , 2012, Current Biology.

[87]  K. Harvey,et al.  The sterile 20-like kinase Tao-1 controls tissue growth by regulating the Salvador-Warts-Hippo pathway. , 2011, Developmental cell.

[88]  P. Bryant,et al.  Drosophila in cancer research: the first fifty tumor suppressor genes , 1994, Journal of Cell Science.

[89]  M. Fuller,et al.  Orientation of Asymmetric Stem Cell Division by the APC Tumor Suppressor and Centrosome , 2003, Science.

[90]  Jada Lewis,et al.  Therapeutic and diagnostic challenges for frontotemporal dementia , 2014, Front. Aging Neurosci..

[91]  N. Perrimon,et al.  The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration , 2010, Development.

[92]  M. Marra,et al.  Cell culture and Drosophila model systems define three classes of anaplastic lymphoma kinase mutations in neuroblastoma , 2012, Disease Models & Mechanisms.

[93]  L. Johnston,et al.  Competitive Interactions Between Cells: Death, Growth, and Geography , 2009, Science.

[94]  C. Doe,et al.  Sgt1 acts via an LKB1/AMPK pathway to establish cortical polarity in larval neuroblasts. , 2012, Developmental biology.

[95]  Byung Hak Kim,et al.  A small-molecule compound identified through a cell-based screening inhibits JAK/STAT pathway signaling in human cancer cells , 2008, Molecular Cancer Therapeutics.

[96]  Lloyd J. Old,et al.  Cancer/testis antigens, gametogenesis and cancer , 2005, Nature Reviews Cancer.

[97]  J. Vincent,et al.  Steep Differences in Wingless Signaling Trigger Myc-Independent Competitive Cell Interactions , 2011, Developmental cell.

[98]  E. Caussinus,et al.  Induction of tumor growth by altered stem-cell asymmetric division in Drosophila melanogaster , 2005, Nature Genetics.

[99]  H. Richardson,et al.  Using Drosophila melanogaster to map human cancer pathways , 2005, Nature Reviews Cancer.

[100]  E. Gateff Malignant neoplasms of genetic origin in Drosophila melanogaster. , 1978, Science.

[101]  M. Amor-Guéret Bloom syndrome, genomic instability and cancer: the SOS-like hypothesis. , 2006, Cancer letters.

[102]  U. Banerjee,et al.  Genetic manipulation of AML1-ETO-induced expansion of hematopoietic precursors in a Drosophila model. , 2010, Blood.

[103]  K. Harvey,et al.  The Salvador–Warts–Hippo pathway — an emerging tumour-suppressor network , 2007, Nature Reviews Cancer.

[104]  D. Wassarman,et al.  A fly's eye view of biology. , 1999, Trends in genetics : TIG.

[105]  A. Spradling,et al.  The adult Drosophila posterior midgut is maintained by pluripotent stem cells , 2006, Nature.

[106]  D. Weil,et al.  CPEB1, a novel gene silenced in gastric cancer: a Drosophila approach , 2011, Gut.

[107]  D. Rossell,et al.  Ectopic Expression of Germline Genes Drives Malignant Brain Tumor Growth in Drosophila , 2010, Science.

[108]  S. Hou,et al.  The adult Drosophila Malpighian tubules are maintained by multipotent stem cells , 2008 .

[109]  H. Carén,et al.  Appearance of the novel activating F1174S ALK mutation in neuroblastoma correlates with aggressive tumor progression and unresponsiveness to therapy. , 2011, Cancer research.

[110]  K. Guillemin,et al.  Transgenic Expression of the Helicobacter pylori Virulence Factor CagA Promotes Apoptosis or Tumorigenesis through JNK Activation in Drosophila , 2012, PLoS pathogens.

[111]  Julia B. Cordero,et al.  APC as a master regulator of intestinal homeostasis and transformation: From flies to vertebrates , 2009, Cell cycle.

[112]  W. Engels,et al.  Evolution of the RECQ family of helicases: A drosophila homolog, Dmblm, is similar to the human bloom syndrome gene. , 1999, Genetics.

[113]  K. Basler,et al.  Loss of PI3K blocks cell-cycle progression in a Drosophila tumor model , 2011, Oncogene.

[114]  C. Klämbt,et al.  Modeling glioma growth and invasion in Drosophila melanogaster. , 2009, Neoplasia.

[115]  B. Edgar,et al.  Cytokine/Jak/Stat Signaling Mediates Regeneration and Homeostasis in the Drosophila Midgut , 2009, Cell.

[116]  C. Micchelli,et al.  Adenomatous polyposis coli regulates Drosophila intestinal stem cell proliferation , 2009, Development.

[117]  D. Glover,et al.  Polo-like kinases: conservation and divergence in their functions and regulation , 2009, Nature Reviews Molecular Cell Biology.

[118]  J. Sklar,et al.  TAN-1, the human homolog of the Drosophila Notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms , 1991, Cell.

[119]  Pier Paolo Di Fiore,et al.  The Tumor Suppressor p53 Regulates Polarity of Self-Renewing Divisions in Mammary Stem Cells , 2009, Cell.

[120]  K. Chang,et al.  Balancing self‐renewal and differentiation by asymmetric division: Insights from brain tumor suppressors in Drosophila neural stem cells , 2012, BioEssays : news and reviews in molecular, cellular and developmental biology.

[121]  C. Nichols,et al.  Human Disease Models in Drosophila melanogaster and the Role of the Fly in Therapeutic Drug Discovery , 2011, Pharmacological Reviews.

[122]  Cayetano Gonzalez Spindle orientation, asymmetric division and tumour suppression in Drosophila stem cells , 2007, Nature Reviews Genetics.

[123]  C. J. Evans,et al.  The Drosophila lymph gland as a developmental model of hematopoiesis , 2005, Development.

[124]  M. D. Golubovsky,et al.  Decrease in the lgl tumor suppressor dose in Drosophila increases survival and longevity in stress conditions , 2006, Experimental Gerontology.

[125]  D. Raben,et al.  A translation inhibitor identified in a Drosophila screen enhances the effect of ionizing radiation and taxol in mammalian models of cancer , 2012, Disease Models & Mechanisms.

[126]  M. Malumbres,et al.  Targeting cell cycle kinases for cancer therapy. , 2007, Current medicinal chemistry.

[127]  G. Morata,et al.  The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc , 2009, Development.

[128]  S. Lens,et al.  The Aurora kinase family in cell division and cancer. , 2008, Biochimica et biophysica acta.

[129]  D. Cleveland,et al.  Losing balance: the origin and impact of aneuploidy in cancer , 2012, EMBO reports.

[130]  N. Perrimon,et al.  Synergy between bacterial infection and genetic predisposition in intestinal dysplasia , 2009, Proceedings of the National Academy of Sciences.

[131]  B. Munos Lessons from 60 years of pharmaceutical innovation , 2009, Nature Reviews Drug Discovery.

[132]  Cayetano Gonzalez,et al.  Centrosome Dysfunction in Drosophila Neural Stem Cells Causes Tumors that Are Not Due to Genome Instability , 2008, Current Biology.

[133]  G. Ruvkun,et al.  A soma-to-germline transformation in long-lived C. elegans mutants , 2009, Nature.

[134]  Juergen A. Knoblich,et al.  Genome-Wide Analysis of Self-Renewal in Drosophila Neural Stem Cells by Transgenic RNAi , 2011, Cell stem cell.

[135]  A. Amon,et al.  Chromosomal instability and aneuploidy in cancer: from yeast to man , 2012, EMBO reports.

[136]  G. Morata,et al.  Cell competition: the embrace of death. , 2007, Developmental cell.

[137]  T. Mak,et al.  DJ-1, a novel regulator of the tumor suppressor PTEN. , 2005, Cancer cell.

[138]  S. Bonaccorsi,et al.  The Drosophila Lkb1 kinase is required for spindle formation and asymmetric neuroblast division , 2007, Development.

[139]  Kevan M. Shokat,et al.  Chemical genetic discovery of targets and anti-targets for cancer polypharmacology , 2012, Nature.

[140]  M. Peifer,et al.  Regulation of Wnt signaling by the tumor suppressor adenomatous polyposis coli does not require the ability to enter the nucleus or a particular cytoplasmic localization , 2012, Molecular biology of the cell.

[141]  C. Nicot,et al.  Current views on the role of Notch signaling and the pathogenesis of human leukemia , 2011, BMC Cancer.

[142]  D. St Johnston,et al.  LKB1 and AMPK maintain epithelial cell polarity under energetic stress , 2013, The Journal of cell biology.

[143]  S. Ohsawa,et al.  Mitochondrial defect drives non-autonomous tumour progression through Hippo signalling in Drosophila , 2012, Nature.

[144]  Crystal M. Botham,et al.  A Transgenic Drosophila Model Demonstrates That the Helicobacter pylori CagA Protein Functions as a Eukaryotic Gab Adaptor , 2008, PLoS pathogens.

[145]  D. Tuveson,et al.  SCRIB expression is deregulated in human prostate cancer, and its deficiency in mice promotes prostate neoplasia. , 2011, The Journal of clinical investigation.

[146]  F. Jackson,et al.  Tumors of the testis and midgut in aging flies , 2008, Fly.

[147]  K. Irvine,et al.  Hippo signaling in Drosophila: Recent advances and insights , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[148]  C. Swanton,et al.  Cancer chromosomal instability: therapeutic and diagnostic challenges , 2012, EMBO reports.

[149]  E. Moreno Is cell competition relevant to cancer? , 2008, Nature Reviews Cancer.

[150]  N. Baker Cell competition , 2011, Current Biology.

[151]  F. Matsuzaki,et al.  The GC kinase Fray and Mo25 regulate Drosophila asymmetric divisions. , 2008, Biochemical and biophysical research communications.

[152]  David Pellman,et al.  A Mechanism Linking Extra Centrosomes to Chromosomal Instability , 2009, Nature.

[153]  J. Gamble,et al.  The Protein Tyrosine Phosphatase Pez Is a Major Phosphatase of Adherens Junctions and Dephosphorylates β-Catenin , 2003 .

[154]  F. Casares,et al.  E-cadherin missense mutations, associated with hereditary diffuse gastric cancer (HDGC) syndrome, display distinct invasive behaviors and genetic interactions with the Wnt and Notch pathways in Drosophila epithelia. , 2006, Human molecular genetics.

[155]  H. Auer,et al.  Aneuploidy-induced delaminating cells drive tumorigenesis in Drosophila epithelia , 2012, Proceedings of the National Academy of Sciences.

[156]  H. Richardson,et al.  An in vivo large-scale chemical screening platform using Drosophila for anti-cancer drug discovery , 2012, Disease Models & Mechanisms.

[157]  M. Malumbres,et al.  From Plk1 to Plk5 , 2011, Cell cycle.

[158]  Investigaciones Científicas,et al.  Epithelial cell polarity, stem cells and cancer , 2012 .

[159]  A. Busturia,et al.  The Polyhomeotic protein induces hyperplastic tissue overgrowth through the activation of the JAK/STAT pathway , 2009, Cell cycle.

[160]  R Berger,et al.  A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. , 1997, Science.

[161]  A. Spradling,et al.  Error-prone polyploid mitosis during normal Drosophila development. , 2010, Genes & development.

[162]  S. Cameron,et al.  Drosophila and mammalian models uncover a role for the myoblast fusion gene TANC1 in rhabdomyosarcoma. , 2012, The Journal of clinical investigation.

[163]  C. Doe,et al.  Drosophila Aurora-A kinase inhibits neuroblast self-renewal by regulating aPKC/Numb cortical polarity and spindle orientation. , 2006, Genes & development.

[164]  M. McVey,et al.  Loss of the bloom syndrome helicase increases DNA ligase 4-independent genome rearrangements and tumorigenesis in aging Drosophila , 2011, Genome Biology.

[165]  G. Klein,et al.  Suppression of Malignancy by Cell Fusion , 1969, Nature.

[166]  A. Krämer,et al.  Centrosome amplification in tumorigenesis. , 2012, Cancer letters.

[167]  T. Halazonetis,et al.  Genomic instability — an evolving hallmark of cancer , 2010, Nature Reviews Molecular Cell Biology.

[168]  P. Walden,et al.  Therapeutic vaccination for cancer immunotherapy: Antigen selection and clinical responses , 2011, Human vaccines.

[169]  Utpal Banerjee,et al.  The hematopoietic stem cell and its niche: a comparative view. , 2007, Genes & development.

[170]  Siqian Feng,et al.  Diverse Tumor Pathology due to Distinctive Patterns of JAK/STAT Pathway Activation Caused by Different Drosophila polyhomeotic Alleles , 2012, Genetics.

[171]  C. Sunkel,et al.  polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. , 1988, Journal of cell science.