Connectivity Map-based discovery of parbendazole reveals targetable human osteogenic pathway

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 41, 2015, Pages 12711-12716

  Brum, Andrea M ^a   Van De Peppel, Jeroen ^a   Van Der Leije, Cindy S ^a   Schreuders Koedam, Marijke ^a   Eijken, Marco ^b   Van Der Eerden, Bram C J ^a   Van Leeuwen, Johannes P T M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b Arcarios BV   (Netherlands)

Author keywords

Connectivity Map; Cytoskeleton; Mesenchymal stem cell; Osteoblast; Osteoporosis

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; BONE SIALOPROTEIN; DEXAMETHASONE; DMH 1; FLUDROCORTISONE; FLUDROXYCORTIDE; FLUMETASONE; FLUNISOLIDE; FLUOCINONIDE; GLUCOCORTICOID RECEPTOR; HALCINONIDE; MIFEPRISTONE; OSTEOPONTIN; PACLITAXEL; PARBENDAZOLE; PROTEIN INHIBITOR; UNCLASSIFIED DRUG; BENZIMIDAZOLE DERIVATIVE; DIFFERENTIATION ANTIGEN;

APOPTOSIS; BONE DEVELOPMENT; BONE MINERALIZATION; CELL DIFFERENTIATION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; COMPUTER MODEL; CONFERENCE PAPER; CONTROLLED STUDY; CYTOSKELETON; DEGRADATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG TARGETING; FOCAL ADHESION; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; IN VITRO STUDY; MARKER GENE; MESENCHYMAL STROMA CELL; MICROTUBULE; MICROTUBULE ASSEMBLY; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; METABOLISM;

ANTIGENS, DIFFERENTIATION; BENZIMIDAZOLES; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; OSTEOGENESIS;

EID: 84944145290     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1501597112     Document Type: Article

References (56)

1. Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 17(12):1726-1733.
2. Kanis JA, Johnell O (2005) Requirements for DXA for the management of osteoporosis in Europe. Osteoporos Int 16(3):229-238.
3. Lamb J, et al. (2006) The Connectivity Map: Using gene-expression signatures to connect small molecules, genes, and disease. Science 313(5795):1929-1935.
4. Qu XA, Rajpal DK (2012) Applications of Connectivity Map in drug discovery and development. Drug Discov Today 17(23-24):1289-1298.
5. Chang M, Smith S, Thorpe A, Barratt MJ, Karim F (2010) Evaluation of phenoxybenzamine in the CFA model of pain following gene expression studies and connectivity mapping. Mol Pain 6:56.
6. Wang G, et al. (2011) Expression-based in silico screening of candidate therapeutic compounds for lung adenocarcinoma. PLoS One 6(1):e14573.
7. Zhong Y, et al. (2013) Renoprotective effect of combined inhibition of angiotensinconverting enzyme and histone deacetylase. J Am Soc Nephrol 24(5):801-811.
8. Koh LW, et al. (2013) A distinct reactive oxygen species profile confers chemoresistance in glioma-propagating cells and associates with patient survival outcome. Antioxid Redox Signal 19(18):2261-2279.
9. Karube K, et al. (2013) Comprehensive gene expression profiles of NK cell neoplasms identify vorinostat as an effective drug candidate. Cancer Lett 333(1):47-55.
10. Havercroft JC, Quinlan RA, Gull K (1981) Binding of parbendazole to tubulin and its influence on microtubules in tissue-culture cells as revealed by immunofluorescence microscopy. J Cell Sci 49:195-204.
11. Marie PJ (2013) Targeting integrins to promote bone formation and repair. Nat Rev Endocrinol 9(5):288-295.
12. Born AK, et al. (2009) Correlating cell architecture with osteogenesis: First steps towards live single cell monitoring. Eur Cell Mater 18(18):49-60, 61-62, discussion 60.
13. Rodríguez JP, González M, Ríos S, Cambiazo V (2004) Cytoskeletal organization of human mesenchymal stem cells (MSC) changes during their osteogenic differentiation. J Cell Biochem 93(4):721-731.
14. Liu H, et al. (2011) Microtubule assembly affects bone mass by regulating both osteoblast and osteoclast functions: Stathmin deficiency produces an osteopenic phenotype in mice. J Bone Miner Res 26(9):2052-2067.
15. Zhao M, et al. (2009) Inhibition of microtubule assembly in osteoblasts stimulates bone morphogenetic protein 2 expression and bone formation through transcription factor Gli2. Mol Cell Biol 29(5):1291-1305.
16. Zilberberg L, Ten Dijke P, Sakai LY, Rifkin DB (2007) A rapid and sensitive bioassay to measure bone morphogenetic protein activity. BMC Cell Biol 8:41.
17. Korchynskyi O, Ten Dijke P (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277(7):4883-4891.
18. Hao J, et al. (2010) In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem Biol 5(2):245-253.
19. Rifas L (2007) The role of noggin in human mesenchymal stem cell differentiation. J Cell Biochem 100(4):824-834.
20. Kaighn ME, Narayan KS, Ohnuki Y, Lechner JF, Jones LW (1979) Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol 17(1):16-23.
21. McKellar QA, Scott EW (1990) The benzimidazole anthelmintic agents-a review. J Vet Pharmacol Ther 13(3):223-247.
22. Davidse LC (1973) Antimitotic activity of methyl benzimidazol-2-yl carbamate (MBC) in Aspergillus nidulans. Pestic Biochem Physiol 3(3):317-325.
23. Davidse LC, Flach W (1977) Differential binding of methyl benzimidazol-2-yl carbamate to fungal tubulin as a mechanism of resistance to this antimitotic agent in mutant strains of Aspergillus nidulans. J Cell Biol 72(1):174-193.
24. Jordan MA, Wilson L (2004) Microtubules as a target for anticancer drugs. Nat Rev Cancer 4(4):253-265.
25. Nogales E, Wang HW (2006) Structural mechanisms underlying nucleotide-dependent self-assembly of tubulin and its relatives. Curr Opin Struct Biol 16(2):221-229.
26. Nogales E, Wang HW (2006) Structural intermediates in microtubule assembly and disassembly: How and why? Curr Opin Cell Biol 18(2):179-184.
27. Gundersen GG, Cook TA (1999) Microtubules and signal transduction. Curr Opin Cell Biol 18(2):179-184.
28. Pockwinse SM, et al. (2006) Microtubule-dependent nuclear-cytoplasmic shuttling of Runx2. J Cell Physiol 206(2):354-362.
29. Chang Y-C, Nalbant P, Birkenfeld J, Chang ZF, Bokoch GM (2008) GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol Biol Cell 19(5):2147-2153.
30. Mathieu PS, Loboa EG (2012) Cytoskeletal and focal adhesion influences on mesenchymal stem cell shape, mechanical properties, and differentiation down osteogenic, adipogenic, and chondrogenic pathways. Tissue Eng Part B Rev 18(6):436-444.
31. Drabek K, Van De Peppel J, Eijken M, Van Leeuwen JP (2011) GPM6B regulates osteoblast function and induction of mineralization by controlling cytoskeleton and matrix vesicle release. J Bone Miner Res 26(9):2045-2051.
32. Kilian KA, Bugarija B, Lahn BT, Mrksich M (2010) Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci USA 107(11):4872-4877.
33. Higuchi C, Nakamura N, Yoshikawa H, Itoh K (2009) Transient dynamic actin cytoskeletal change stimulates the osteoblastic differentiation. J Bone Miner Metab 27(2):158-167.
34. Chen Q, et al. (2014) An osteopontin-integrin interaction plays a critical role in directing adipogenesis and osteogenesis by mesenchymal stem cells. Stem Cells 32(2):327-337.
35. Biggs MJ, Richards RG, Dalby MJ (2010) Nanotopographical modification: A regulator of cellular function through focal adhesions. Nanomedicine (Lond) 6(5):619-633.
36. Gupton SL, Waterman-Storer CM (2006) Spatiotemporal feedback between actomyosin and focal-adhesion systems optimizes rapid cell migration. Cell 125(7):1361-1374.
37. Ingber DE (2006) Cellular mechanotransduction: Putting all the pieces together again. FASEB J 20(7):811-827.
38. Ingber DE (1993) Cellular tensegrity: Defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104(Pt 3):613-627.
39. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS (2004) Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6(4):483-495.
40. Zhao M, et al. (2006) The zinc finger transcription factor Gli2 mediates bone morphogenetic protein 2 expression in osteoblasts in response to hedgehog signaling. Mol Cell Biol 26(16):6197-6208.
41. Phimphilai M, Zhao Z, Boules H, Roca H, Franceschi RT (2006) BMP signaling is required for RUNX2-dependent induction of the osteoblast phenotype. J Bone Miner Res 21(4):637-646.
42. Noël D, et al. (2004) Short-term BMP-2 expression is sufficient for in vivo osteochondral differentiation of mesenchymal stem cells. Stem Cells 22(1):74-85.
43. Gazzerro E, Canalis E (2006) Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord 7(1-2):51-65.
44. Lavery K, Swain P, Falb D, Alaoui-Ismaili MH (2008) BMP-2/4 and BMP-6/7 differentially utilize cell surface receptors to induce osteoblastic differentiation of human bone marrow-derived mesenchymal stem cells. J Biol Chem 283(30):20948-20958.
45. Lecanda F, Avioli LV, Cheng SL (1997) Regulation of bone matrix protein expression and induction of differentiation of human osteoblasts and human bone marrow stromal cells by bone morphogenetic protein-2. J Cell Biochem 67(3):386-396.
46. Cruz AC, Silva ML, Caon T, Simões CM (2012) Addition of bone morphogenetic protein type 2 to ascorbate and β-glycerophosphate supplementation did not enhance osteogenic differentiation of human adipose-derived stem cells. J Appl Oral Sci 20(6):628-635.
47. Diefenderfer DL, Osyczka AM, Reilly GC, Leboy PS (2003) BMP responsiveness in human mesenchymal stem cells. Connect Tissue Res 44(Suppl 1):305-311.
48. Fu R, et al. (2013) Effectiveness and harms of recombinant human bone morphogenetic protein-2 in spine fusion: A systematic review and meta-analysis. Ann Intern Med 158(12):890-902.
49. Simmonds MC, et al. (2013) Safety and effectiveness of recombinant human bone morphogenetic protein-2 for spinal fusion: A meta-analysis of individual-participant data. Ann Intern Med 158(12):877-889.
50. Eijken M, et al. (2007) The activin A-follistatin system: Potent regulator of human extracellular matrix mineralization. FASEB J 21(11):2949-2960.
51. Bruedigam C, et al. (2011) Basic techniques in human mesenchymal stem cell cultures: differentiation into osteogenic and adipogenic lineages, genetic perturbations, and phenotypic analyses. Curr Protoc Stem Cell Biol Chapter 1: Unit 1 H.3.
52. Igathinathane C, Pordesimo LO, Columbus EP, Batchelor WD, Methuku SR (2008) Shape identification and particles size distribution from basic shape parameters using ImageJ. Comput Electron Agric 63(2):168-182.
53. Du P, Kibbe WA, Lin SM (2008) lumi: A pipeline for processing Illumina microarray. Bioinformatics 24(13):1547-1548.
54. Smyth GK (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3(3):e3.
55. Eijken M, et al. (2006) The essential role of glucocorticoids for proper human osteoblast differentiation and matrix mineralization. Mol Cell Endocrinol 248(1-2):87-93.
56. Chiba H, Sawada N, Ono T, Ishii S, Mori M (1993) Establishment and characterization of a simian virus 40-immortalized osteoblastic cell line from normal human bone. Jpn J Cancer Res 84(3):290-297.