Vav3 collaborates with p190-BCR-ABL in lymphoid progenitor leukemogenesis, proliferation, and survival

Blood

Volumn 120, Issue 4, 2012, Pages 800-811

  Chang, Kyung Hee ^a,b   Sanchez Aguilera, Abel ^c   Shen, Shuhong ^d   Sengupta, Amitava ^a   Madhu, Malav N ^a   Ficker, Ashley M ^a   Dunn, Susan K ^b   Kuenzi, Ashley M ^a   Arnett, Jorden L ^a   Santho, Rebecca A ^a   Agirre, Xabier ^e   Perentesis, John P ^f   Deininger, Michael W ^g   Zheng, Yi ^a   Bustelo, Xose R ^h   Williams, David A ^c   Cancelas, Jose A ^a,b  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^e UNIVERSITY CLINIC OF NAVARRA   (Spain)

^f CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^g UNIVERSITY OF UTAH   (United States)

^h Centro de Investigacion del Cancer   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BCR ABL PROTEIN; CRK LIKE PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; P21 ACTIVATED KINASE; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN P190; PROTEIN TYROSINE KINASE INHIBITOR; PROTEIN VAV3; RAC2 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VAV PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LEUKEMOGENESIS; LYMPHOCYTE PROLIFERATION; LYMPHOID PROGENITOR CELL; MOUSE; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

EID: 84864445261     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-06-361709     Document Type: Article

References (50)

1. Daley GQ, Van Etten RA, Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science. 1990;247(4944):824-830.
2. Castor A, Nilsson L, Astrand-Grundstrom I, et al. Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nat Med. 2005;11(6):630-637. (Pubitemid 40868303)
3. Kantarjian H, Pasquini R, Hamerschlak N, et al. Dasatinib or high-dose imatinib for chronic-phase chronic myeloid leukemia after failure of first-line imatinib: a randomized phase 2 trial. Blood. 2007;109(12):5143-5150. (Pubitemid 46890528)
4. Nicolini FE, Mauro MJ, Martinelli G, et al. Epidemiologic study on survival of chronic myeloid leukemia and Ph(+) acute lymphoblastic leukemia patients with BCR-ABL T315I mutation. Blood. 2009;114(26):5271-5278.
5. Kantarjian H, Shah NP, Hochhaus A, et al. Dasatinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2010;362(24):2260-2270.
6. Notta F, Mullighan CG, Wang JC, et al. Evolution of human BCR-ABL1 lymphoblastic leukaemia-initiating cells. Nature. 2011;469(7330):362-367.
7. Harnois T, Constantin B, Rioux A, Grenioux E, Kitzis A, Bourmeyster N. Differential interaction and activation of Rho family GTPases by p210bcr-abl and p190bcr-abl. Oncogene. 2003;22(41):6445-6454. (Pubitemid 37281691)
8. Sahay S, Pannucci NL, Mahon GM, et al. The RhoGEF domain of p210 Bcr-Abl activates RhoA and is required for transformation. Oncogene. 2008;27(14):2064-2071. (Pubitemid 351442739)
9. Thomas EK, Cancelas JA, Chae HD, et al. Rac guanosine triphosphatases represent integrating molecular therapeutic targets for BCR-ABL-induced myeloproliferative disease. Cancer Cell. 2007;12(5):467-478. (Pubitemid 350046406)
10. Sengupta A, Arnett J, Dunn S, Williams DA, Cancelas JA. Rac2 GTPase deficiency depletes BCR-ABL+ leukemic stem cells and progenitors in vivo. Blood. 2010;116(1):81-84.
11. Diebold BA, Bokoch GM. Molecular basis for Rac2 regulation of phagocyte NADPH oxidase. Nat Immunol. 2001;2(3):211-215. (Pubitemid 33705996)
12. Rassool FV, Gaymes TJ, Omidvar N, et al. Reactive oxygen species, DNA damage, and error-prone repair: a model for genomic instability with progression in myeloid leukemia? Cancer Res. 2007;67(18):8762-8771. (Pubitemid 47437452)
13. Tybulewicz VL. Vav-family proteins in T-cell signalling. Curr Opin Immunol. 2005;17(3):267-274. (Pubitemid 40692661)
14. Bustelo XR. Regulation of Vav proteins by intramolecular events. Front Biosci. 2002;7:d24-30.
15. Movilla N, Bustelo XR. Biological and regulatory properties of Vav-3, a new member of the Vav family of oncoproteins. Mol Cell Biol. 1999;19(11):7870-7885. (Pubitemid 29493450)
16. Fujikawa K, Miletic AV, Alt FW, et al. Vav1/2/3-null mice define an essential role for Vav family proteins in lymphocyte development and activation but a differential requirement in MAPK signaling in T and B cells. J Exp Med. 2003;198(10):1595-1608. (Pubitemid 37467173)
17. Bassermann F, Jahn T, Miething C, et al. Association of Bcr-Abl with the proto-oncogene Vav is implicated in activation of the Rac-1 pathway. J Biol Chem. 2002;277(14):12437-12445. (Pubitemid 34952818)
18. Roberts AW, Kim C, Zhen L, et al. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity. 1999;10(2):183-196. (Pubitemid 29115624)
19. Williams DA, Tao W, Yang F, et al. Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood. 2000;96(5):1646-1654. (Pubitemid 30661042)
20. Matsuguchi T, Inhorn RC, Carlesso N, Xu G, Druker B, Griffin JD. Tyrosine phosphorylation of p95Vav in myeloid cells is regulated by GM-CSF, IL-3 and steel factor and is constitutively increased by p210BCR/ABL. EMBO J. 1995;14(2):257-265.
21. Williams RT, Roussel MF, Sherr CJ. Arf gene loss enhances oncogenicity and limits imatinib response in mouse models of Bcr-Abl-induced acute lymphoblastic leukemia. Proc Natl Acad Sci U S A. 2006;103(17):6688-6693.
22. Bustelo XR, Ledbetter JA, Barbacid M. Product of vav proto-oncogene defines a new class of tyrosine protein kinase substrates. Nature. 1992; 356(6364):68-71.
23. Gu Y, Jia B, Yang FC, et al. Biochemical and biological characterization of a human Rac2 GTPase mutant associated with phagocytic immunodeficiency. J Biol Chem. 2001;276(19):15929-15938.
24. Cho YJ, Zhang B, Kaartinen V, et al. Generation of rac3 null mutant mice: role of Rac3 in Bcr/Abl-caused lymphoblastic leukemia. Mol Cell Biol. 2005;25(13):5777-5785. (Pubitemid 40853609)
25. Cragg MS, Harris C, Strasser A, Scott CL. Unleashing the power of inhibitors of oncogenic kinases through BH3 mimetics. Nat Rev Cancer. 2009;9(5):321-326.
26. Schürmann A, Mooney AF, Sanders LC, et al. p21-activated kinase 1 phosphorylates the death agonist bad and protects cells from apoptosis. Mol Cell Biol. 2000;20(2):453-461. (Pubitemid 30023086)
27. Datta SR, Dudek H, Tao X, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell. 1997;91(2):231-241. (Pubitemid 27456390)
28. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms. Science. 1999;286(5443):1358-1362.
29. Harada H, Becknell B, Wilm M, et al. Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase A. Mol Cell. 1999;3(4):413-422. (Pubitemid 29292598)
30. Alvarado Y, Apostolidou E, Swords R, Giles FJ. Emerging therapeutic options for Philadelphia-positive acute lymphocytic leukemia. Expert Opin Emerg Drugs. 2007;12(1):165-179. (Pubitemid 46504909)
31. Kardinal C, Konkol B, Schulz A, et al. Cell-penetrating SH3 domain blocker peptides inhibit proliferation of primary blast cells from CML patients. Faseb J. 2000;14(11):1529-1538. (Pubitemid 30636557)
32. Mishra S, Zhang B, Cunnick JM, Heisterkamp N, Groffen J. Resistance to imatinib of bcr/abl p190 lymphoblastic leukemia cells. Cancer Res. 2006;66(10):5387-5393. (Pubitemid 43844965)
33. del Pozo MA, Schwartz MA, Hu J, Kiosses WB, Altman A, Villalba M. Guanine exchange-dependent and -independent effects of Vav1 on integrin-induced T cell spreading. J Immunol. 2003;170(1):41-47. (Pubitemid 36026121)
34. Salomoni P, Wasik MA, Riedel RF, et al. Expression of constitutively active Raf-1 in the mitochondria restores antiapoptotic and leukemogenic potential of a transformation-deficient BCR/ABL mutant. J Exp Med. 1998;187(12):1995-2007. (Pubitemid 28285569)
35. Janumyan YM, Sansam CG, Chattopadhyay A, et al. Bcl-xL/Bcl-2 coordinately regulates apoptosis, cell cycle arrest and cell cycle entry. EMBO J. 2003;22(20):5459-5470. (Pubitemid 37279955)
36. Letai A, Bassik MC, Walensky LD, Sorcinelli MD, Weiler S, Korsmeyer SJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2002;2(3):183-192. (Pubitemid 41043974)
37. Gregory MA, Phang TL, Neviani P, et al. Wnt/Ca2+/NFAT signaling maintains survival of Ph+leukemia cells upon inhibition of Bcr-Abl. Cancer Cell. 2010;18(1):74-87.
38. Yang FC, Kapur R, King AJ, et al. Rac2 stimulates Akt activation affecting BAD/Bcl-XL expression while mediating survival and actin function in primary mast cells. Immunity. 2000;12(5):557-568.
39. Chattopadhyay A, Chiang CW, Yang E. BAD/BCL-[X(L)] heterodimerization leads to bypass of G0/G1 arrest. Oncogene. 2001;20(33):4507-4518. (Pubitemid 32772433)
40. Cotteret S, Jaffer ZM, Beeser A, Chernoff J. p21-activated kinase 5 (Pak5) localizes to mitochondria and inhibits apoptosis by phosphorylating BAD. Mol Cell Biol. 2003;23(16):5526-5539. (Pubitemid 36951321)
41. Jin S, Zhuo Y, Guo W, Field J. p21-activated Kinase 1 (Pak1)-dependent phosphorylation of Raf-1 regulates its mitochondrial localization, phosphorylation of BAD, and Bcl-2 association. J Biol Chem. 2005;280(26):24698- 24705. (Pubitemid 40934559)
42. Sells MA, Knaus UG, Bagrodia S, Ambrose DM, Bokoch GM, Chernoff J. Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr Biol. 1997;7(3):202-210. (Pubitemid 27164726)
43. Schultz KR, Bowman WP, Aledo A, et al. Improved early event-free survival with imatinib in Philadelphia chromosome-positive acute lymphoblastic leukemia: a children's oncology group study. J Clin Oncol. 2009;27(31):5175-5181.
44. Weisberg E, Choi HG, Ray A, et al. Discovery of a small-molecule type II inhibitor of wild-type and gatekeeper mutants of BCR-ABL, PDGFRalpha, Kit, and Src kinases: novel type II inhibitor of gatekeeper mutants. Blood. 2010;115(21):4206-4216.
45. Azam M, Nardi V, Shakespeare WC, et al. Activity of dual SRC-ABL inhibitors highlights the role of BCR/ABL kinase dynamics in drug resistance. Proc Natl Acad Sci U S A. 2006;103(24):9244-9249. (Pubitemid 43902563)
46. Talpaz M, Shah NP, Kantarjian H, et al. Dasatinib in imatinib-resistant Philadelphia chromosome-positive leukemias. N Engl J Med. 2006;354(24):2531- 2541. (Pubitemid 43882349)
47. Lilly MB, Ottmann OG, Shah NP, et al. Dasatinib 140 mg once daily versus 70 mg twice daily in patients with Ph-positive acute lymphoblastic leukemia who failed imatinib: Results from a phase 3 study. Am J Hematol. 2010;85(3):164-170.
48. Kuroda J, Puthalakath H, Cragg MS, et al. Bim and Bad mediate imatinib-induced killing of Bcr/Abl+ leukemic cells, and resistance due to their loss is overcome by a BH3 mimetic. Proc Natl Acad Sci U S A. 2006;103(40):14907-14912. (Pubitemid 44527827)
49. Williams RT, den Besten W, Sherr CJ. Cytokine-dependent imatinib resistance in mouse BCR-ABL+, Arf-null lymphoblastic leukemia. Genes Dev. 2007;21(18):2283-2287. (Pubitemid 47443334)
50. Sengupta A, Ficker AM, Dunn SK, Madhu M, Cancelas JA. Bmi1 reprograms CML B-lymphoid progenitors to become B-ALL-initiating cells. Blood. 2012;119(2):494-502.