Pten regulates homeostasis and inflammation-induced migration of myelocytes in zebrafish

Journal of Hematology and Oncology

Volumn 7, Issue 1, 2014, Pages

  Dong, Zhi Wei ^a   Ren, Chun Guang ^a   Xia, Yu ^a   Su, Dan ^a   Du, Ting Ting ^b   Fan, Hong Bo ^a   Yuan, Hao ^b   Wang, Lei ^a   Dong, Mei ^a   Li, Wei Chun ^a   Jin, Yi ^b   Chen, Yi ^b   Deng, Min ^a   Liu, Ting Xi ^a   Gu, Ai Hua ^c   Zhou, Yong ^a  

^a UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

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

^c NANJING MEDICAL UNIVERSITY   (China)

Author keywords

cebpa; Definitive myelopoiesis; Myeloid cells; pten; Zebrafish

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL MATURATION; CELL MIGRATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME INHIBITION; GENE; GENE EXPRESSION; GENE LOSS; GENE OVEREXPRESSION; HEMATOPOIESIS; HOMEOSTASIS; IMMUNOFLUORESCENCE; IN SITU HYBRIDIZATION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; MOLECULAR MECHANICS; MUTANT; MYELOID PROGENITOR CELL; NEUTROPHIL; NONHUMAN; PTEN GENE; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; APOPTOSIS; CELL GROWTH; CELL MOTION; CYTOLOGY; METABOLISM; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CELL GROWTH PROCESSES; CELL MOVEMENT; HOMEOSTASIS; INFLAMMATION; MYELOID CELLS; PTEN PHOSPHOHYDROLASE; ZEBRAFISH;

EID: 84898036350     PISSN: None     EISSN: 17568722     Source Type: Journal    
DOI: 10.1186/1756-8722-7-17     Document Type: Article

References (58)

1. PTEN loss in the continuum of common cancers, rare syndromes and mouse models. Hollander MC, Blumenthal GM, Dennis PA, Nat Rev Cancer 2011 11 289 301 10.1038/nrc3037 21430697
2. PTEN (MMAC1) mutations are frequent in primary glioblastomas (de novo) but not in secondary glioblastomas. Tohma Y, Gratas C, Biernat W, Peraud A, Fukuda M, Yonekawa Y, Kleihues P, Ohgaki H, J Neuropathol Exp Neurol 1998 57 684 689 10.1097/00005072-199807000-00005 9690672
3. High frequency of PTEN, PI3K, and AKT abnormalities in T-cell acute lymphoblastic leukemia. Gutierrez A, Sanda T, Grebliunaite R, Carracedo A, Salmena L, Ahn Y, Dahlberg S, Neuberg D, Moreau LA, Winter SS, Larson R, Zhang J, Protopopov A, Chin L, Pandolfi PP, Silverman LB, Hunger SP, Sallan SE, Look AT, Blood 2009 114 647 650 10.1182/blood-2009-02-206722 19458356
4. The PTEN, Mdm2, p53 tumor suppressor-oncoprotein network. Mayo LD, Donner DB, Trends Biochem Sci 2002 27 462 467 10.1016/S0968-0004(02)02166-7 12217521
5. Tumor suppressor PTEN: modulator of cell signaling, growth, migration and apoptosis. Yamada KM, Araki M, J Cell Sci 2001 114 Pt 13 2375 2382 11559746
6. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT, Haug JS, Rupp D, Porter-Westpfahl KS, Wiedemann LM, Wu H, Li L, Nature 2006 441 518 522 10.1038/nature04747 16633340
7. Pten dependence distinguishes haematopoietic stem cells from leukaemia-initiating cells. Yilmaz OH, Valdez R, Theisen BK, Guo W, Ferguson DO, Wu H, Morrison SJ, Nature 2006 441 475 482 10.1038/nature04703 16598206
8. mTOR activation induces tumor suppressors that inhibit leukemogenesis and deplete hematopoietic stem cells after Pten deletion. Lee JY, Nakada D, Yilmaz OH, Tothova Z, Joseph NM, Lim MS, Gilliland DG, Morrison SJ, Cell Stem Cell 2010 7 593 605 10.1016/j.stem.2010.09.015 21040901
9. Distinct and dynamic requirements for mTOR signaling in hematopoiesis and leukemogenesis. Kentsis A, Look AT, Cell Stem Cell 2012 11 281 282 10.1016/j.stem.2012.08.007 22958924
10. mTOR complex 1 plays critical roles in hematopoiesis and Pten-loss-evoked leukemogenesis. Kalaitzidis D, Sykes SM, Wang Z, Punt N, Tang Y, Ragu C, Sinha AU, Lane SW, Souza AL, Clish CB, Anastasiou D, Gilliland DG, Scadden DT, Guertin DA, Armstrong SA, Cell Stem Cell 2012 11 429 439 10.1016/j.stem.2012.06.009 22958934
11. McBindall-a better name for CCAAT/enhancer binding proteins? McKnight SL, Cell 2001 107 259 261 10.1016/S0092-8674(01)00543-8 11701103
12. Dominant-negative C/ebp and polycomb group protein Bmi1 extend short-lived hematopoietic stem/progenitor cell life span and induce lethal dyserythropoiesis. Zhou T, Wang L, Zhu K, Dong M, Xu P-F, Chen Y, Chen S-J, Chen Z, Deng M, Liu TX, Blood 2011 118 3842 3852 10.1182/blood-2010-12-327908 21828130
13. Biallelic mutations in the CEBPA gene and low CEBPA expression levels as prognostic markers in intermediate-risk AML. Van Doorn SBVW, Erpelinck C, Meijer J, van Oosterhoud S, Van Putten WL, Valk PJ, Berna BH, Tenen DG, Lowenberg B, Delwel R, Hematol J Off J Eur Haematol Assoc 2003 4 31 40
14. Dominant-negative mutations of CEBPA, encoding CCAAT/enhancer binding protein- (C/EBP), in acute myeloid leukemia. Pabst T, Mueller BU, Zhang P, Radomska HS, Narravula S, Schnittger S, Behre G, Hiddemann W, Tenen DG, Nat Genet 2001 27 263 270 10.1038/85820 11242107
15. Mutations in the gene encoding the transcription factor CCAAT/enhancer binding protein in myelodysplastic syndromes and acute myeloid leukemias. Gombart AF, Hofmann W-K, Kawano S, Takeuchi S, Krug U, Kwok SH, Larsen RJ, Asou H, Miller CW, Hoelzer D, Koeffler HP, Blood 2002 99 1332 1340 10.1182/blood.V99.4.1332 11830484
16. Favorable prognostic significance of CEBPA mutations in patients with de novo acute myeloid leukemia: a study from the Acute Leukemia French Association (ALFA). Preudhomme C, Sagot C, Boissel N, Cayuela J-M, Tigaud I, de Botton S, Thomas X, Raffoux E, Lamandin C, Castaigne S, Fenaux P, Dombret H, ALFA Group, Blood 2002 100 2717 2723 10.1182/blood-2002-03-0990 12351377
17. Absence of granulocyte colony-stimulating factor signaling and neutrophil development in CCAAT enhancer binding protein alpha-deficient mice. Zhang DE, Zhang P, Wang ND, Hetherington CJ, Darlington GJ, Tenen DG, Proc Natl Acad Sci U S A 1997 94 569 574 10.1073/pnas.94.2.569 9012825
18. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Zhang P, Iwasaki-Arai J, Iwasaki H, Fenyus ML, Dayaram T, Owens BM, Shigematsu H, Levantini E, Huettner CS, Lekstrom-Himes JA, Akashi K, Tenen DG, Immunity 2004 21 853 863 10.1016/j.immuni.2004.11.006 15589173
19. Transcription factors, normal myeloid development, and leukemia. Tenen DG, Hromas R, Licht JD, Zhang D-E, Blood 1997 90 489 519 9226149
20. Use of RDA analysis of knockout mice to identify myeloid genes regulated in vivo by PU. 1 and C/EBP Iwama A, Zhang P, Darlington GJ, McKercher SR, Maki R, Tenen DG, Nucleic Acids Res 1998 26 3034 3043 10.1093/nar/26.12.3034 9611252
21. CCAAT/enhancer binding protein is a regulatory switch sufficient for induction of granulocytic development from bipotential myeloid progenitors. Radomska HSH, Huettner CSCCS, Zhang PU, Cheng TAO, Scadden DT, Tenen DG, Mol Cell Biol 1998 18 4301 4314 9632814
22. C/EBPalpha bypasses granulocyte colony-stimulating factor signals to rapidly induce PU.1 gene expression, stimulate granulocytic differentiation, and limit proliferation in 32D cl3 myeloblasts. Wang X, Scott E, Sawyers CL, Friedman AD, Blood 1999 94 560 571 10397723
23. An evolutionarily conserved PTEN-C/EBPalpha-CTNNA1 axis controls myeloid development and transformation. Fu C-T, Zhu K-Y, Mi J-Q, Liu Y-F, Murray ST, Fu Y-F, Ren C-G, Dong Z-W, Liu Y-J, Dong M, Jin Y, Chen Y, Deng M, Zhang W, Chen B, Breslin P, Chen S-J, Chen Z, Becker MW, Zhu J, Zhang J-W, Liu TX, Blood 2010 115 4715 4724 10.1182/blood-2009-11-255778 20371743
24. The "definitive" (and "primitive") guide to zebrafish hematopoiesis. Davidson AJ, Zon LI, Oncogene 2004 23 7233 7246 10.1038/sj.onc.1207943 15378083
25. Use of the zebrafish system to study primitive and definitive hematopoiesis. De Jong JLO, Zon LI, Annu Rev Genet 2005 39 481 501 10.1146/annurev.genet.39.073003.095931 16285869
26. Zebrafish blood stem cells. Chen AT, Zon LI, J Cell Biochem 2009 108 35 42 10.1002/jcb.22251 19565566
27. Novel insights into the genetic controls of primitive and definitive hematopoiesis from zebrafish models. Sood R, Liu P, Adv Hematol 2012 2012 830703 22888355
28. Ptena and ptenb genes play distinct roles in zebrafish embryogenesis. Croushore JA, Blasiole B, Riddle RC, Thisse C, Thisse B, Canfield VA, Robertson GP, Cheng KC, Levenson R, Dev Dyn 2005 234 911 921 10.1002/dvdy.20576 16193492
29. Zebrafish pten genes have overlapping and non-redundant functions in tumorigenesis and embryonic development. Faucherre A, Taylor GS, Overvoorde J, Dixon JE, Den HJ, Oncogene 2008 27 1079 1086 10.1038/sj.onc.1210730 17704803
30. Pten is essential for embryonic development and tumour suppression. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP, Nat Genet 1998 19 348 355 10.1038/1235 9697695
31. In vivo interstitial migration of primitive macrophages mediated by JNK-matrix metalloproteinase 13 signaling in response to acute injury. Zhang Y, Bai X-T, Zhu K-Y, Jin Y, Deng M, Le H-Y, Fu Y-F, Chen Y, Zhu J, Look AT, Kanki J, Chen Z, Chen S-J, Liu TX, J Immunol 2008 181 2155 2164 18641354
32. Origins and unconventional behavior of neutrophils in developing zebrafish. Le Guyader D, Redd MJ, Colucci-Guyon E, Murayama E, Kissa K, Briolat V, Mordelet E, Zapata A, Shinomiya H, Herbomel P, Blood 2008 111 132 141 10.1182/blood-2007-06-095398 17875807
33. Irf8 regulates macrophage versus neutrophil fate during zebrafish primitive myelopoiesis. Li L, Jin H, Xu J, Shi Y, Wen Z, Blood 2011 117 1359 1369 10.1182/blood-2010-06-290700 21079149
34. Resolution of inflammation by retrograde chemotaxis of neutrophils in transgenic zebrafish. Mathias JR, Perrin BJ, Liu T, Kanki J, Look AT, Huttenlocher A, J Leukoc Biol 2006 80 1281 1288 10.1189/jlb.0506346 16963624
35. Zebrafish granulocyte colony-stimulating factor receptor signaling promotes myelopoiesis and myeloid cell migration. Liongue C, Hall CJ, O'Connell BA, Crosier P, Ward AC, Blood 2009 113 2535 2546 10.1182/blood-2008-07-171967 19139076
36. Simultaneous intravital imaging of macrophage and neutrophil behaviour during inflammation using a novel transgenic zebrafish. Gray C, Loynes CA, Whyte MKB, Crossman DC, Renshaw SA, Chico TJ A, Thromb Haemost 2011 105 811 819 10.1160/TH10-08-0525 21225092
37. Cannabinoid receptor 2 suppresses leukocyte inflammatory migration by modulating the JNK/c-Jun/Alox5 pathway. Liu Y-J, Fan H-B, Jin Y, Ren C-G, Jia X-E, Wang L, Chen Y, Dong M, Zhu K-Y, Dong Z-W, Ye B-X, Zhong Z, Deng M, Liu TX, Ren R, J Biol Chem 2013 288 13551 13562 10.1074/jbc.M113.453811 23539630
38. TSC1-TSC2: a complex tale of PKB-mediated S6K regulation. McManus EJ, Alessi DR, Nat Cell Biol 2002 4 214 E216 10.1038/ncb0902-e214 12205484
39. The paradox of Akt-mTOR interactions. Vadlakonda L, Dash A, Pasupuleti M, Anil Kumar K, Reddanna P, Front Oncol 2013 3 165 23802099
40. C/EBPalpha induces PU.1 and interacts with AP-1 and NF-kappaB to regulate myeloid development. Friedman AD, Blood Cells Mol Dis 2007 39 340 343 10.1016/j.bcmd.2007.06.010 17669672
41. Tenets of PTEN tumor suppression. Salmena L, Carracedo A, Pandolfi PP, Cell 2008 133 403 414 10.1016/j.cell.2008.04.013 18455982
42. Ptenb mediates gastrulation cell movements via Cdc42/AKT1 in zebrafish. Yeh C-M, Liu Y-C, Chang C-J, Lai S-L, Hsiao C-D, Lee S-J, PLoS One 2011 6 18702 10.1371/journal.pone.0018702 21494560
43. Loss of Pten promotes angiogenesis and enhanced vegfaa expression in zebrafish. Choorapoikayil S, Weijts B, Kers R, de Bruin A, den Hertog J, Dis Model Mech 2013 6 5 1159 1166 10.1242/dmm.012377 23720233
44. Phagocyte partnership during the onset and resolution of inflammation. Soehnlein O, Lindbom L, Nat Rev Immunol 2010 10 427 439 10.1038/nri2779 20498669
45. Tumor suppressor PTEN is a physiologic suppressor of chemoattractant- mediated neutrophil functions. Subramanian KK, Jia Y, Zhu D, Simms BT, Jo H, Hattori H, You J, Mizgerd JP, Luo HR, Blood 2007 109 4028 4037 10.1182/blood-2006-10-055319 17202315
46. Myeloid PTEN promotes inflammation but impairs bactericidal activities during murine pneumococcal pneumonia. Schabbauer G, Matt U, Günzl P, Warszawska J, Furtner T, Hainzl E, Elbau I, Mesteri I, Doninger B, Binder BR, Knapp S, J Immunol 2010 185 468 476 10.4049/jimmunol.0902221 20505137
47. Pivotal role of Pten in the balance between proliferation and differentiation of hematopoietic stem cells in zebrafish. Choorapoikayil S, Kers R, Herbomel P, Kissa K, den Hertog J, Blood 2014 123 184 190 10.1182/blood-2013-05-501544 24124088
48. The inositol 3-phosphatase PTEN negatively regulates Fc gamma receptor signaling, but supports Toll-like receptor 4 signaling in murine peritoneal macrophages. Cao X, Wei G, Fang H, Guo J, Weinstein M, Marsh CB, Ostrowski MC, Tridandapani S, J Immunol 2004 172 4851 4857 15067063
49. PTEN limits alveolar macrophage function against Pseudomonas aeruginosa after bone marrow transplantation. Hubbard LLN, Wilke CA, White ES, Moore BB, Am J Respir Cell Mol Biol 2011 45 1050 1058 10.1165/rcmb.2011-0079OC 21527775
50. PTEN directly activates the actin depolymerization factor cofilin-1 during PGE2-mediated inhibition of phagocytosis of fungi. Serezani CH, Kane S, Medeiros AI, Cornett AM, Kim S-H, Marques MM, Lee S-P, Lewis C, Bourdonnay E, Ballinger MN, White ES, Peters-Golden M, Sci Signal 2012 5 a12 22317922
51. Targeting the phosphoinositide 3-kinase pathway in hematologic malignancies. Jabbour E, Ottmann OG, Deininger M, Hochhaus A, Haematologica 2014 99 7 18 10.3324/haematol.2013.087171 24425689
52. Translational control of C/EBPalpha and C/EBPbeta isoform expression. Calkhoven CF, Müller C, Leutz A, Genes Dev 2000 14 1920 1932 10921906
53. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. Arsham AM, Howell JJ, Simon MC, J Biol Chem 2003 278 29655 29660 10.1074/jbc.M212770200 12777372
54. Stages of embryonic development of the zebrafish. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, Dev Dyn 1995 203 253 310 10.1002/aja.1002030302 8589427
55. High-resolution in situ hybridization to whole-mount zebrafish embryos. Thisse C, Thisse B, Nat Protoc 2008 3 59 69 10.1038/nprot.2007.514 18193022
56. Zebrafish early macrophages colonize cephalic mesenchyme and developing brain, retina, and epidermis through a M-CSF receptor-dependent invasive process. Herbomel P, Thisse B, Thisse C, Dev Biol 2001 238 274 288 10.1006/dbio.2001.0393 11784010
57. A developmental transition in growth control during zebrafish caudal fin development. Goldsmith MI, Iovine MK, O'Reilly-Pol T, Johnson SL, Dev Biol 2006 296 450 457 10.1016/j.ydbio.2006.06.010 16844108
58. Transient and stable transgenesis using tol2 transposon vectors. Kikuta H, Kawakami K, Methods Mol Biol 2009 546 69 84 10.1007/978-1-60327-977-2-5 19378098