Functional CSF-1 receptors are located at the nuclear envelope and activated via the p110δ isoform of PI 3-kinase

FASEB Journal

Volumn 26, Issue 2, 2012, Pages 691-706

  Zwaenepoel, Olivier ^a   Tzenaki, Niki ^a   Vergetaki, Aikaterini ^a   Makrigiannakis, Antonis ^a   Vanhaesebroeck, Bart ^b   Papakonstanti, Evangelia A ^a  

^a UNIVERSITY OF CRETE   (Greece)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

CSF 1R; Nucleus; p110 ; PI3K; Rab5

Indexed keywords

COLONY STIMULATING FACTOR 1; COLONY STIMULATING FACTOR 1 RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P27; RAB PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL NUCLEUS MEMBRANE; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INACTIVATION; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ANIMALS; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CYCLIN-DEPENDENT KINASE INHIBITOR P27; FEMALE; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; MICE, KNOCKOUT; NUCLEAR ENVELOPE; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RAB5 GTP-BINDING PROTEINS; RECEPTOR, MACROPHAGE COLONY-STIMULATING FACTOR; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION;

EID: 84856544134     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-189753     Document Type: Article

References (60)

1. Stanley, E. R., Chen, D. M., and Lin, H. S. (1978) Induction of macrophage production and proliferation by a purified colony stimulating factor. Nature 274, 168-170 (Pubitemid 8374441)
2. Stanley, E. R., Berg, K. L., Einstein, D. B., Lee, P. S., Pixley, F. J., Wang, Y., and Yeung, Y. G. (1997) Biology and action of colony-stimulating factor-1. Mol. Reprod. Dev. 46, 4-10 (Pubitemid 27021347)
3. Rettenmier, C. W., Chen, J. H., Roussel, M. F., and Sherr, C. J. (1985) The product of the c-fms proto-oncogene: a glycoprotein with associated tyrosine kinase activity. Science 228, 320-322 (Pubitemid 15076827)
4. Rettenmier, C. W., Sacca, R., Furman, W. L., Roussel, M. F., Holt, J. T., Nienhuis, A. W., Stanley, E. R., and Sherr, C. J. (1986) Expression of the human c-fms proto-oncogene product (colony-stimulating factor-1 receptor) on peripheral blood mononuclear cells and choriocarcinoma cell lines. J. Clin. Invest. 77, 1740-1746 (Pubitemid 16062624)
5. Yeung, Y. G., Jubinsky, P. T., Sengupta, A., Yeung, D. C., and Stanley, E. R. (1987) Purification of the colony-stimulating factor 1 receptor and demonstration of its tyrosine kinase activity. Proc. Natl. Acad. Sci. U. S. A. 84, 1268-1271 (Pubitemid 17027334)
6. Sherr, C. J., Rettenmier, C. W., Sacca, R., Roussel, M. F., Look, A., and Stanley, E. R. (1985) The c-fms proto-oncogene product is related to the receptor for the mononuclear phagocyte growth factor, CSF-1. Cell 41, 665-676 (Pubitemid 15243374)
7. Kacinski, B. M. (1997) CSF-1 and its receptor in breast carcinomas and neoplasms of the female reproductive tract. Mol. Reprod. Dev. 46, 71-74
8. Ide, H., Seligson, D. B., Memarzadeh, S., Xin, L., Horvath, S., Dubey, P., Flick, M. B., Kacinski, B. M., Palotie, A., and Witte, O. N. (2002) Expression of colony-stimulating factor 1 receptor during prostate development and prostate cancer progression. Proc. Natl. Acad. Sci. U. S. A. 99, 14404-14409 (Pubitemid 35257684)
9. Kluger, H. M., Dolled-Filhart, M., Rodov, S., Kacinski, B. M., Camp, R. L., and Rimm, D. L. (2004) Macrophage colony-stimulating factor-1 receptor expression is associated with poor outcome in breast cancer by large cohort tissue microarray analysis. Clin. Cancer Res. 10, 173-177 (Pubitemid 38114176)
10. Toy, E. P., Azodi, M., Folk, N. L., Zito, C. M., Zeiss, C. J., and Chambers, S. K. (2009) Enhanced ovarian cancer tumorigenesis and metastasis by the macrophage colony-stimulating factor. Neoplasia 11, 136-144
11. Kirma, N., Hammes, L. S., Liu, Y.-G., Nair, H. B., Valente, P. T., Kumar, S., Flowers, L. C., and Tekmal, R. R. (2007) Elevated expression of the oncogene c-fms and its ligand, the macrophage colony-stimulating factor-1, in cervical cancer and the role of transforming growth factor-β1 in inducing c-fms expression. Cancer Res. 67, 1918-1926 (Pubitemid 46424207)
12. Kacinski, B. M., Carter, D., Kohorn, E. I., Mittal, K., Bloodgood, R. S., Donahue, J., Kramer, C. A., Fischer, D., Edwards, R., Chambers, S. K., Chambers, J. T., and Schwartz, P. E. (1989) Oncogene expression in vivo by ovarian adenocarcinomas and mixed-mullerian tumors. Yale J. Biol. Med. 62, 379-392 (Pubitemid 20005030)
13. Bingle, L., Brown, N. J., and Lewis, C. E. (2002) The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies. J. Pathol. 196, 254-265 (Pubitemid 34189413)
14. Tang, R., Beuvon, F., Ojeda, M., Mosseri, V., Pouillart, P., and Scholl, S. (1992) M-CSF (monocyte colony stimulating factor) and M-CSF receptor expression by breast tumour cells: M-CSF mediated recruitment of tumour infiltrating monocytes? J. Cell. Biochem. 50, 350-356 (Pubitemid 23005801)
15. Guilbert, L. J., and Stanley, E. R. (1986) The interaction of 125I-colony-stimulating factor-1 with bone marrow- derived macrophages. J. Biol. Chem. 261, 4024-4032 (Pubitemid 17198829)
16. Yeung, Y.-G., Wang, Y., Einstein, D. B., Lee, P. S. W., and Stanley, E. R. (1998) Colony-stimulating factor-1 stimulates the formation of multimeric cytosolic complexes of signaling proteins and cytoskeletal components in macrophages. J. Biol. Chem. 273, 17128-17137 (Pubitemid 28311749)
17. Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M., and Bilanges, B. (2010) The emerging mechanisms of isoform-specific PI3K signalling. Nat. Rev. Mol. Cell. Biol. 11, 329-341
18. Papakonstanti, E. A., Ridley, A. J., and Vanhaesebroeck, B. (2007) The p110- isoform of PI 3-kinase negatively controls RhoA and PTEN. EMBO J. 26, 3050-3061 (Pubitemid 47057501)
19. Papakonstanti, E. A., Zwaenepoel, O., Bilancio, A., Burns, E., Nock, G. E., Houseman, B., Shokat, K., Ridley, A. J., and Vanhaesebroeck, B. (2008) Distinct roles of class IA PI 3-kinase isoforms in primary and immortalised macrophages. J. Cell. Sci. 121, 4124-4133
20. Fujita, N., Sato, S., Katayama, K., and Tsuruo, T. (2002) Akt-dependent phosphorylation of p27Kip1 promotes binding to 14-3-3 and cytoplasmic localization. J. Biol. Chem. 277, 28706-28713
21. Murayama, T., Yokode, M., Kataoka, H., Imabayashi, T., Yoshida, H., Sano, H., Nishikawa, S., Nishikawa, S.-I., and Kita, T. (1999) Intraperitoneal administration of anti-c-fms monoclonal antibody prevents initial events of atherogenesis but does not reduce the size of advanced lesions in apolipoprotein E-deficient mice. Circulation 99, 1740-1746 (Pubitemid 29162488)
22. Yu, W., Chen, J., Xiong, Y., Pixley, F. J., Dai, X. M., Yeung, Y. G., and Stanley, E. R. (2008) CSF-1 receptor structure/function in MacCsf1r-/- macrophages: regulation of proliferation, differentiation, and morphology. J. Leukoc. Biol. 84, 852-863
23. Liu, J., Lamb, D., Chou, M. M., Liu, Y.-J., and Li, G. (2007) Nerve growth factor-mediated neurite outgrowth via regulation of Rab5. Mol. Biol. Cell 18, 1375-1384 (Pubitemid 46626632)
24. Brock, T. G., Paine, R., and Peters-Golden, M. (1994) Localization of 5-lipoxygenase to the nucleus of unstimulated rat basophilic leukemia cells. J. Biol. Chem. 269, 22059-22066 (Pubitemid 24282128)
25. Dignam, J. D., Lebovitz, R., and Roeder, R. (1983) Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489
26. Nagata, Y., Lan, K.-H., Zhou, X., Tan, M., Esteva, F. J., Sahin, A. A., Klos, K. S., Li, P., Monia, B. P., Nguyen, N. T., Hortobagyi, G. N., Hung, M.-C., and Yu, D. (2004) PTEN activation contributes to tumor inhibition by trastuzumab, and loss of PTEN predicts trastuzumab resistance in patients. Cancer Cell. 6, 117-127 (Pubitemid 39485684)
27. Payrastre, B., Nievers, M., Boonstra, J., Breton, M., Verkleij, A. J., and Van Bergen en Henegouwen, P. M. (1992) A differential location of phosphoinositide kinases, diacylglycerol kinase, and phospholipase C in the nuclear matrix. J. Biol. Chem. 267, 5078-5084
28. Cao, H., Lei, Z. M., Bian, L., and Rao, C. V. (1995) Functional nuclear epidermal growth factor receptors in human choriocarcinoma JEG-3 cells and normal human placenta. Endocrinology 136, 3163-3172
29. Niswender, K. D., Gallis, B., Blevins, J. E., Corson, M. A., Schwartz, M. W., and Baskin, D. G. (2003) Immunocytochemical detection of phosphatidylinositol 3-kinase activation by insulin and leptin. J. Histochem. Cytochem. 51, 275-283 (Pubitemid 36245983)
30. Cress. A. E. (2000) Quantitation of phosphotyrosine signals in human prostate cell adhesion sites. BioTechniques 29, 776-779
31. Robertson, D., Savage, K., Reis-Filho, J., and Isacke, C. (2008) Multiple immunofluorescence labelling of formalin-fixed paraffin-embedded (FFPE) tissue. BMC Cell Biol. 9, 13
32. Okkenhaug, K., Bilancio, A., Farjot, G., Priddle, H., Sancho, S., Peskett, E., Pearce, W., Meek, S. E., Salpekar, A., Waterfield, M. D., Smith, A. J. H., and Vanhaesebroeck, B. (2002) Impaired B and T cell antigen receptor signaling in p110δ PI 3-kinase mutant mice. Science 297, 1031-1034 (Pubitemid 34856039)
33. Lee, P. S., Wang, Y., Dominguez, M. G., Yeung, Y. G., Murphy, M. A., Bowtell, D. D., and E.R., S. (1999) The Cbl protooncoprotein stimulates CSF-1 receptor multiubiquitination and endocytosis, and attenuates macrophage proliferation. EMBO J. 18, 3616-3628 (Pubitemid 29308842)
34. Vlcek, S., Dechat, T., and Foisner, R. (2001) Nuclear envelope and nuclear matrix: interactions and dynamics. Cell. Mol. Life Sci. 58, 1758-1765 (Pubitemid 33108766)
35. Stuurman, N., Meijne, A. M., van der Pol, A. J., de Jong, L., van Driel, R., and van Renswoude, J. (1990) The nuclear matrix from cells of different origin. Evidence for a common set of matrix proteins. J. Biol. Chem. 265, 5460-5465
36. Martelli, A. M., Manzoli, L., and Cocco, L. (2004) Nuclear inositides: facts and perspectives. Pharmacol. Ther. 101, 47-64 (Pubitemid 38068525)
37. Martelli, A. M., Faenza, I., Billi, A. M., Manzoli, L., Evangelisti, C., Fala, F., and Cocco, L. (2006) Intranuclear 3′-phosphoinositide metabolism and Akt signaling: New mechanisms for tumorigenesis and protection against apoptosis? Cell. Signal. 18, 1101-1107 (Pubitemid 43674029)
38. Stenmark, H., Vitale, G., Ullrich, O., and Zerial, M. (1995) Rabaptin-5 is a direct effector of the small GTPase Rab5 in endocytic membrane fusion. Cell 83, 423-432
39. Stenmark, H., Parton, R., Steele-Mortimer, O., Lütcke, A., Gruenberg, J., and Zerial, M. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296 (Pubitemid 24090209)
40. Rosenfeld, J. L., Moore, R. H., Zimmer, K. P., Alpizar-Foster, E., Dai, W., Zarka, M. N., and Knoll, B. J. (2001) Lysosome proteins are redistributed during expression of a GTP-hydrolysis-defective rab5a. J. Cell Sci. 114, 4499-4508 (Pubitemid 34082870)
41. Wainszelbaum, M. J., Proctor, B. M., Pontow, S. E., Stahl, P. D., and Barbieri, M. A. (2006) IL4/PGE2 induction of an enlarged early endosomal compartment in mouse macrophages is Rab5-dependent. Exp. Cell Res. 312, 2238-2251 (Pubitemid 43949509)
42. Małecki, J., Wiedłocha, A., Wesche, J., and Olsnes, S. (2002) Vesicle transmembrane potential is required for translocation to the cytosol of externally added FGF-1. EMBO J. 21, 4480-4490 (Pubitemid 34984335)
43. Małecki, J., Wesche, J., Skjerpen, C., Wiedłocha, A., and Olsnes, S. (2004) Translocation of FGF-1 and FGF-2 across vesicular membranes occurs during G1-phase by a common mechanism. Mol. Biol. Cell 15, 801-814 (Pubitemid 38146494)
44. Wesche, J., Wiedłocha, A., Falnes, P. O., Choe, S., and Olsnes, S. (2000) Externally added aFGF mutants do not require extensive unfolding for transport to the cytosol and the nucleus in NIH/3T3 cells. Biochemistry 39, 15091-15100
45. Gorvel, J.-P., Chavrier, P., Zerial, M., and Gruenberg, J. (1991) rab5 controls early endosome fusion in vitro. Cell 64, 915-925 (Pubitemid 121001179)
46. Bucci, C., Parton, R. G., Mather, I. H., Stunnenberg, H., Simons, K., Hoflack, B., and Zerial, M. (1992) The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728
47. Stenmark, H., Parton, R. G., Steele-Mortimer, O., Lütcke, A., Gruenberg, J., and M., Z. (1994) Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J. 13, 1287-1296 (Pubitemid 24090209)
48. Stenmark, H., Aasland, R., Toh, B.-H., and D'Arrigo, A. (1996) Endosomal localization of the autoantigen EEA1 is mediated by a zinc-binding FYVE finger. J. Biol. Chem. 271, 24048-24054
49. Mills, I. G., Jones, A. T., and Clague, M. J. (1998) Involvement of the endosomal autoantigen EEA1 in homotypic fusion of early endosomes. Curr. Biol. 8, 881-884 (Pubitemid 28356049)
50. Simonsen, A., Lippé, R., Christoforidis, S., Gaullier, J. M., Brech, A., Callaghan, J., Toh, B. H., Murphy, C., Zerial, M., and Stenmark, H. (1998) EEA1 links PI(3)K function to Rab5 regulation of endosome fusion. Nature 394, 494-498 (Pubitemid 28373962)
51. Shin, H.-W., Hayashi, M., Christoforidis, S., Lacas-Gervais, S., Hoepfner, S., Wenk, M. R., Modregger, J., Uttenweiler-Joseph, S., Wilm, M., Nystuen, A., Frankel, W. N., Solimena, M., De Camilli, P., and Zerial, M. (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J. Cell Biol. 170, 607-618 (Pubitemid 41186935)
52. Patel, S., and Player, M. R. (2009) Colony-stimulating factor-1 receptor inhibitors for the treatment of cancer and inflammatory disease. Curr. Top. Med. Chem. 9, 599-610
53. Ohno, H., Kubo, K., Murooka, H., Kobayashi, Y., Nishitoba, T., Shibuya, M., Yoneda, T., and Isoe, T. (2006) A c-fms tyrosine kinase inhibitor, Ki20227, suppresses osteoclast differentiation and osteolytic bone destruction in a bone metastasis model. Mol. Cancer Ther. 5, 2634-2643 (Pubitemid 44848990)
54. Conway, J. G., McDonald, B., Parham, J., Keith, B., Rusnak, D. W., Shaw, E., Jansen, M., Lin, P., Payne, A., Crosby, R. M., Johnson, J. H., Frick, L., Lin, M.-H. J., Depee, S., Tadepalli, S., Votta, B., James, I., Fuller, K., Chambers, T. J., Kull, F. C., Chamberlain, S. D., and Hutchins, J. T. (2005) Inhibition of colony-stimulating-factor-1 signaling in vivo with the orally bioavailable cFMS kinase inhibitor GW2580. Proc. Natl. Acad. Sci. U. S. A. 102, 16078-16083 (Pubitemid 41552870)
55. Smalley Jr., T. L., Chamberlain, S. D., Mills, W. Y., Musso, D. L., Randhawa, S. A., Ray, J. A., Samano, V., and Frick, L. (2007) Synthesis of novel anilinoquinolines as c-fms inhibitors. Bioorg. Med. Chem. Lett. 17, 6257-6260 (Pubitemid 47552819)
56. Irvine, K. M., Burns, C. J., Wilks, A. F., Su, S., Hume, D. A., and Sweet, M. J. (2006) A CSF-1 receptor kinase inhibitor targets effector functions and inhibits pro-inflammatory cytokine production from murine macrophage populations. FASEB J. 20, 1921-1923
57. Patch, R. J., Brandt, B. M., Asgari, D., Baindur, N., Chadha, N. K., Georgiadis, T., Cheung, W. S., Petrounia, I. P., Donatelli, R. R., Chaikin, M. A., and Player, M. R. (2007) Potent 2′-aminoanilide inhibitors of cFMS as potential anti-inflammatory agents. Bioorg. Med. Chem. Lett. 17, 6070-6074 (Pubitemid 47552848)
58. Illig, C. R., Chen, J., Wall, M. J., Wilson, K. J., Ballentine, S. K., Rudolph, M. J., DesJarlais, R. L., Chen, Y., Schubert, C., Petrounia, I., Crysler, C. S., Molloy, C. J., Chaikin, M. A., Manthey, C. L., Player, M. R., Tomczuk, B. E., and Meegalla, S. K. (2008) Discovery of novel FMS kinase inhibitors as anti-inflammatory agents. Bioorg. Med. Chemi. Lett. 18, 1642-1648 (Pubitemid 351343803)
59. Wall, M. J., Chen, J., Meegalla, S., Ballentine, S. K., Wilson, K. J., DesJarlais, R. L., Schubert, C., Chaikin, M. A., Crysler, C., Petrounia, I. P., Donatelli, R. R., Yurkow, E. J., Boczon, L., Mazzulla, M., Player, M. R., Patch, R. J., Manthey, C. L., Molloy, C., Tomczuk, B., and Illig, C. R. (2008) Synthesis and evaluation of novel 3,4,6-substituted 2-quinolones as FMS kinase inhibitors. Bioorg. Med. Chem. Lett. 18, 2097-2102 (Pubitemid 351391842)
60. Huang, H., Hutta, D. A., Hu, H., DesJarlais, R. L., Schubert, C., Petrounia, I. P., Chaikin, M. A., Manthey, C. L., and Player, M. R. (2008) Design and synthesis of a pyrido[2,3-d]pyrimidin-5-one class of anti-inflammatory FMS inhibitors. Bioorg. Med. Chem. Lett. 18, 2355-2361 (Pubitemid 351447286)