Suppression of PDGF-induced PI3 kinase activity by imatinib promotes adipogenesis and adiponectin secretion

Journal of Molecular Endocrinology

Volumn 48, Issue 3, 2012, Pages 229-240

  Fitter, Stephen ^a   Vandyke, Kate ^a   Gronthos, Stan ^b,c   Zannettino, Andrew C W ^a,c  

^a INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

^b Mesenchymal Stem Cell Group   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; IMATINIB; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR;

ADIPOCYTE; ADIPOGENESIS; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MESENCHYMAL STROMA CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ADIPOCYTES; ADIPOGENESIS; ADIPONECTIN; CELL DIFFERENTIATION; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; ENZYME ACTIVATION; HUMANS; HYDRAZONES; MESENCHYMAL STROMAL CELLS; MITOGENS; MOLECULAR WEIGHT; PHOSPHATIDYLINOSITOL 3-KINASES; PIPERAZINES; PLATELET-DERIVED GROWTH FACTOR; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PYRIMIDINES; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; SULFONAMIDES;

EID: 84861144839     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-12-0003     Document Type: Article

References (57)

1. Aouadi M, Jager J, Laurent K, Gonzalez T, Cormont M, Binetruy B, Le Marchand-Brustel Y, Tanti JF & Bost F. 2007 P38MAP kinase activity is required for human primary adipocyte differentiation. FEBS Letters 581 5591-5596. (doi:10.1016/j.febslet.2007.10.064)
2. Artemenko Y, Gagnon A, Aubin D & Sorisky A 2005 Anti-adipogenic effect of PDGF is reversed by PKC inhibition. Journal of Cellular Physiology 204 646-653. (doi:10.1002/jcp.20314)
3. Bonner JC 2010 Mesenchymal cell survival in airway and interstitial pulmonary fibrosis. Fibrogenesis & Tissue Repair 3 15. (doi:10.1186/1755-1536-3-15)
4. Breccia M, Muscaritoli M, Aversa Z, Mandelli F & Alimena G 2004 Imatinib mesylate may improve fasting blood glucose in diabetic PhC chronic myelogenous leukemia patients responsive to treatment. Journal of Clinical Oncology 22 4653-4655. (doi:10.1200/JCO.2004.04.217)
5. Breccia M, Muscaritoli M & Alimena G 2005 Reduction of glycosylated hemoglobin with stable insulin levels in a diabetic patient with chronic myeloid leukemia responsive to imatinib. Haematologica 90(Suppl) ECR21.
6. Buchdunger E, Cioffi CL, Law N, Stover D, Ohno-Jones S, Druker BJ & Lydon NB 2000 Abl protein-tyrosine kinase inhibitor STI571 inhibits in vitro signal transduction mediated by c-kit and plateletderived growth factor receptors. Journal of Pharmacology and Experimental Therapeutics 295 139-145.
7. Chaudhary LR, Hofmeister AM & Hruska KA 2004 Differential growth factor control of bone formation through osteoprogenitor differentiation. Bone 34 402-411. (doi:10.1016/j.bone.2003.11.014)
8. Chaussade C, Rewcastle GW, Kendall JD, Denny WA, Cho K, Gronning LM, Chong ML, Anagnostou SH, Jackson SP, Daniele N et al. 2007 Evidence for functional redundancy of class IA PI3K isoforms in insulin signalling. Biochemical Journal 404 449-458. (doi:10.1042/BJ20070003)
9. le Coutre P, Kreuzer KA, Pursche S, Bonin M, Leopold T, Baskaynak G, Dorken B, Ehninger G, Ottmann O, Jenke A et al. 2004 Pharmacokinetics and cellular uptake of imatinib and its mainmetabolite CGP74588. Cancer Chemotherapy and Pharmacology 53 313-323. (doi:10.1007/s00280-003-0741-6)
10. Dewar AL, Cambareri AC, Zannettino AC, Miller BL, Doherty KV, Hughes TP & Lyons AB 2005 Macrophage colony-stimulating factor receptor c-fms is a novel target of imatinib. Blood 105 3127-3132.(doi:10.1182/blood-2004-10-3967)
11. Dewar AL, Farrugia AN, Condina MR, Bik To L, Hughes TP, Vernon-Roberts B & Zannettino AC 2006 Imatinib as a potentialantiresorptive therapy for bone disease. Blood 107 4334-4337.(doi:10.1182/blood-2005-09-3568)
12. Druker BJ 2004 Imatinib as a paradigm of targeted therapies. Advances in Cancer Research 91 1-30. (doi:10.1016/S0065-230X(04)91001-9)
13. Fierro F, Illmer T, Jing D, Schleyer E, Ehninger G, Boxberger S & Bornhauser M 2007 Inhibition of platelet-derived growth factor receptorb by imatinib mesylate suppresses proliferation and alters differentiation of human mesenchymal stem cells in vitro. Cell Proliferation 40 355-366. (doi:10.1111/j.1365-2184.2007.00438.x)
14. Fitter S, Dewar AL, Kostakis P, To LB, Hughes TP, Roberts MM, Lynch K, Vernon-Roberts B & Zannettino AC 2008 Long-term imatinib therapy promotes bone formation in CML patients. Blood 111 2538-2547. (doi:10.1182/blood-2007-07-104281)
15. Fitter S, Vandyke K, Schultz CG, White D, Hughes TP & Zannettino AC 2010 Plasma adiponectin levels are markedly elevated in imatinibtreated chronic myeloid leukemia (CML) patients: a mechanism for improved insulin sensitivity in type 2 diabetic CML patients? Journal of Clinical Endocrinology and Metabolism 95 3763-3767.(doi:10.1210/jc.2010-006)
16. Gagnon A, Landry A & Sorisky A 2009 IKKb and the anti-adipogenic effect of platelet-derived growth factor in human abdominal subcutaneous preadipocytes. Journal of Endocrinology 201 75-80.(doi:10.1677/JOE-08-0411)
17. Gimble J 1998 Marrow stromal adipocytes. In Marrow Stromal Cell Culture, pp 67-87. Eds JN Beresford & ME Owen. Cambridge: Cambridge University Press.
18. Gologan R, Constantinescu G, Georgescu D, Ostroveanu D, Vasilache D, Dobrea C, Iancu D & Popov V 2009 Hypolipemiant besides antileukemic effect of imatinib mesylate. Leukemia Research 33 1285-1287. (doi:10.1016/j.leukres.2009.02.024)
19. Greenberger JS 1979 Corticosteroid-dependent differentiation of human marrow preadipocytes in vitro. In Vitro 15 823-828.(doi:10.1007/BF02618309)
20. Hagerkvist R, Sandler S, Mokhtari D & Welsh N 2007 Amelioration ofdiabetes by imatinib mesylate (Gleevec): role of b-cell NF-kappaBactivation and anti-apoptotic preconditioning. FASEB Journal 21 618-628. (doi:10.1096/fj.06-6910com)
21. Han MS, Chung KW, Cheon HG, Rhee SD, Yoon CH, Lee MK, Kim KW and Lee MS 2009 Imatinib mesylate reduces endoplasmic reticulum stress and induces remission of diabetes in db/db mice. Diabetes 58 329-336. (doi:10.2337/db08-0080)
22. Hay N & Sonenberg N 2004 Upstream and downstream of m TOR. Genes and Development 18 1926-1945. (doi:10.1101/gad.1212704)
23. Hock JM & Canalis E 1994 Platelet-derived growth factor enhances bone cell replication, but not differentiated function of osteoblasts. Endocrinology 134 1423-1428. (doi:10.1210/en.134.3.1423)
24. Isenmann S, Arthur A, Zannettino AC, Turner JL, Shi S, Glackin CA & Gronthos S 2009 TWIST family of basic helix-loop-helix transcriptionfactors mediate human mesenchymal stem cell growthand commitment. Stem Cells 27 2457-2468. (doi:10.1002/stem.181)
25. Jaiswal RK, Jaiswal N, Bruder SP, Mbalaviele G, Marshak DR & Pittenger MF 2000 Adult human mesenchymal stem cell differentiation to the osteogenic or adipogenic lineage is regulated by mitogen-activated protein kinase. Journal of Biological Chemistry 275 9645-9652. (doi:10.1074/jbc.275.13.9645)
26. Jonsson S, Olsson B, Ohlsson C, Lorentzon M, Mellstrom D & Wadenvik H 2008 Increased cortical bone mineralization inimatinib treated patients with chronic myelogenous leukemia. Haematologica 93 1101-1103. (doi:10.3324/haematol.12373)
27. Jonsson S, Hjorth-Hansen H, Olsson B, Wadenvik H, Sundan A & Standal T 2012 Imatinib inhibits proliferation of human mesenchymal stem cells and promotes early but not late osteoblast differentiation in vitro. Journal of Bone and Mineral Metabolism 30 119-123. (doi:10.1007/s00774-011-0323-3)
28. Justesen J, Mosekilde L, Holmes M, Stenderup K, Gasser J, Mullins JJ, Seckl JR & Kassem M 2004 Mice deficient in 11b-hydroxysteroid dehydrogenase type 1 lack bone marrow adipocytes, but maintain normal bone formation. Endocrinology 145 1916-1925.(doi:10.1210/en.2003-1427)
29. Kohn AD, Summers SA, Birnbaum MJ & Roth RA 1996 Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. Journal of Biological Chemistry 271 31372-31378. (doi:10.1074/jbc.271.49.31372)
30. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M & Mann M 2005 Mechanism of divergent growth factor effects in mesenchymalstem cell differentiation. Science 308 1472-1477. (doi:10.1126/science.1107627)
31. Kubota K, Sakikawa C, Katsumata M, Nakamura T & Wakabayashi K 2002 Platelet-derived growth factor BB secreted from osteoclasts acts as an osteoblastogenesis inhibitory factor. Journal of Bone and Mineral Research 17 257-265. (doi:10.1359/jbmr.2002.17.2.257)
32. Lara-Castro C, Luo N, Wallace P, Klein RL and Garvey WT. 2006 Adiponectinmultimeric complexes and the metabolic syndrome trait cluster. Diabetes 55 249-259. (doi:10.2337/diabetes.55.01.06.db05-1105)
33. Lehmann JM, Lenhard JM, Oliver BB, Ringold GM & Kliewer SA 1997 Peroxisome proliferator-activated receptors a and gamma are activated by indomethacin and other non-steroidal anti-inflammatory drugs. Journal of Biological Chemistry 272 3406-3410.(doi:10.1074/jbc.272.6.3406)
34. Li S, Shin HJ, Ding EL & van Dam RM2009 Adiponectin levels and risk of type 2 diabetes: a systematic review and meta-analysis. Journal of the American Medical Association 302 179-188. (doi:10.1001/jama.2009.976)
35. Louvet C, Szot GL, Lang J, Lee MR, Martinier N, Bollag G, Zhu S, Weiss A & Bluestone JA 2008 Tyrosine kinase inhibitors reversetype 1 diabetes in nonobese diabetic mice. PNAS 105 18895-18900.(doi:10.1073/pnas.0810246105)
36. Magun R, Burgering BM, Coffer PJ, Pardasani D, Lin Y, Chabot J & Sorisky A 1996 Expression of a constitutively activated form of protein kinase B (c-Akt) in 3T3-L1 preadipose cells causes spontaneous differentiation. Endocrinology 137 3590-3593.(doi:10.1210/en.137.8.3590)
37. Mariani S, Tornaghi L, Sassone M, Basciani S, Buzzetti R, Gambacorti-Passerini C, Spera G & Gnessi L 2010 Imatinib does not substantially modify the glycemic profile in patients with chronic myeloid leukaemia. Leukemia Research 34 e5-e7. (doi:10.1016/j.leukres.2009.08.003)
38. Martin SK, Fitter S, Bong LF, Drew JJ, Gronthos S, Shepherd PR and Zannettino AC 2010 NVP-BEZ235, a dual pan class I PI3 kinase andmTOR inhibitor, promotes osteogenic differentiation in human mesenchymal stromal cells. Journal of Bone and Mineral Research 25 2126-2137. (doi:10.1002/jbmr.114)
39. Miki H, Yamauchi T, Suzuki R, Komeda K, Tsuchida A, Kubota N, Terauchi Y, Kamon J, Kaburagi Y, Matsui J et al. 2001 Essential role of insulin receptor substrate 1 (IRS-1) and IRS-2 in adipocyte differentiation. Molecular and Cellular Biology 21 2521-2532.(doi:10.1128/MCB.21.7.2521-2532.2001)
40. Nawrocki AR, Rajala MW, Tomas E, Pajvani UB, Saha AK, Trumbauer ME, Pang Z, Chen AS, Ruderman NB, Chen H et al. 2006 Mice lacking adiponectin show decreased hepatic insulin sensitivity and reduced responsiveness to peroxisome proliferator-activated receptor gamma agonists. Journal of Biological Chemistry 281 2654-2660. (doi:10.1074/jbc.M505311200)
41. O'Sullivan S, Horne A, Wattie D, Porteous F, Callon K, Gamble G, Ebeling P, Browett P & Grey A 2009 Decreased bone turnover despite persistent secondary hyperparathyroidism during prolonged treatment with imatinib. Journal of Clinical Endocrinology and Metabolism 94 1131-1136. (doi:10.1210/jc.2008-2324)
42. Phillips SA, Ciaraldi TP, Kong AP, Bandukwala R, Aroda V, Carter L, Baxi S, Mudaliar SR & Henry RR 2003 Modulation of circulatingand adipose tissue adiponectin levels by antidiabetic therapy. Diabetes 52 667-674. (doi:10.2337/diabetes.52.3.667)
43. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S & Marshak DR 1999 Multilineage potential of adult human mesenchymal stem cells. Science 284 143-147. (doi:10.1126/science.284.5411.143)
44. Sakaue H, Ogawa W, Matsumoto M, Kuroda S, Takata M, Sugimoto T, Spiegelman BM & Kasuga M 1998 Posttranscriptional control ofadipocyte differentiation through activation of phosphoinositide 3-kinase. Journal ofBiologicalChemistry 273 28945-28952. (doi:10.1074/jbc.273.44.28945)
45. Scavo LM, Karas M, Murray M & Leroith D 2004 Insulin-like growth factor-I stimulates both cell growth and lipogenesis during differentiation of human mesenchymal stem cells into adipocytes. Journal of Clinical Endocrinology and Metabolism 89 3543-3553.(doi:10.1210/jc.2003-031682)
46. Serra V, Markman B, Scaltriti M, Eichhorn PJ, Valero V, Guzman M, Botero ML, Llonch E, Atzori F, Di Cosimo S et al. 2008 NVP-BEZ235, a dual PI3K/mTOR inhibitor, prevents PI3K signaling and inhibits the growth of cancer cells with activating PI3K mutations. Cancer Research 68 8022-8030. (doi:10.1158/0008-5472.CAN-08-1385)
47. Tokunaga A, Oya T, Ishii Y, Motomura H, Nakamura C, Ishizawa S, Fujimori T, Nabeshima Y, Umezawa A, Kanamori M, et al. 2008 PDGF receptor b is a potent regulator of mesenchymal stromal cell function. Journal of Bone and Mineral Research 23 1519-1528. (doi:10.1359/jbmr.080409)
48. Tsapas A, Vlachaki E, Sarigianni M, Klonizakis F & Paletas K 2008 Restoration of insulin sensitivity following treatment with imatinib mesylate (Gleevec) in non-diabetic patients with chronic myelogenic leukemia (CML). Leukemia Research 32 674-675. (doi:10.1016/j.leukres.2007.08.014)
49. Vandyke K, Dewar AL, Diamond P, Fitter S, Schultz CG, Sims NA & Zannettino AC 2010a The tyrosine kinase inhibitor dasatinib dysregulates bone remodeling through inhibition of osteoclasts in vivo. Journal of Bone and Mineral Research 25 1759-1770.(doi:10.1002/jbmr.85)
50. Vandyke K, Fitter S, Dewar AL, Hughes TP & Zannettino AC 2010b Dysregulation of bone remodeling by imatinib mesylate. Blood 115 766-774. (doi:10.1182/blood-2009-08-237404)
51. Veneri D, Franchini M & Bonora E 2005 Imatinib and regression of type 2 diabetes. New England Journal of Medicine 352 1049-1050. (doi:10.1056/NEJM200503103521023)
52. Waki H, Yamauchi T, Kamon J, Ito Y, Uchida S, Kita S, Hara K, Hada Y, Vasseur F, Froguel P et al. 2003 Impaired multimerization of human adiponectin mutants associated with diabetes. Molecular structure and multimer formation of adiponectin. Journal of Biological Chemistry 278 40352-40363. (doi:10.1074/jbc.M300365200)
53. Wang Y, Lam KS, Chan L, Chan KW, Lam JB, Lam MC, Hoo RC, Mak WW, Cooper GJ & Xu A 2006 Post-translational modifications of the four conserved lysine residues within the collagenous domain of adiponectin are required for the formation of its high molecular weight oligomeric complex. Journal of Biological Chemistry 281 16391-16400. (doi:10.1074/jbc.M513907200)
54. Wu X, Chen S, Orlando SA, Yuan J, Kim ET, Munugalavadla V, Mali RS, Kapur R & Yang FC 2011 P85a regulates osteoblast differentiation by cross-talking with the MAPK pathway. Journal of Biological Chemistry 286 13512-13521. (doi:10.1074/jbc.M110.187351)
55. Xu J & Liao K 2004 Protein kinase B/AKT 1 plays a pivotal role in insulin-like growth factor-1 receptor signaling induced 3T3-L1 adipocyte differentiation. Journal of Biological Chemistry 279 35914-35922. (doi:10.1074/jbc.M402297200)
56. Yamauchi T, Kamon J, Waki H, Murakami K, Motojima K, Komeda K, Ide T, Kubota N, Terauchi Y, Tobe K et al. 2001 The mechanisms by which both heterozygous peroxisome proliferator-activated receptor gamma (PPARgamma) deficiency and PPARgamma agonist improve insulin resistance. Journal of Biological Chemistry 276 41245-41254. (doi:10.1074/jbc.M103241200)
57. Zhao JJ, Cheng H, Jia S, Wang L, Gjoerup OV, Mikami A & Roberts TM 2006 The p110a isoform of PI3K is essential for proper growth factor signaling and oncogenic transformation. PNAS 103 16296-16300. (doi:10.1073/pnas.0607899103)