Activation of the IGF1 pathway mediates changes in cellular contractility and motility in single-suture craniosynostosis

Journal of Cell Science

Volumn 129, Issue 3, 2016, Pages 483-491

  Al Rekabi, Zeinab ^a,b   Wheeler, Marsha M ^c   Leonard, Andrea ^a   Fura, Adriane M ^c   Juhlin, Ilsa ^a   Frazar, Christopher ^c   Smith, Joshua D ^c   Park, Sarah S ^b   Gustafson, Jennifer A ^b   Clarke, Christine M ^b   Cunningham, Michael L ^b,d   Sniadecki, Nathan J ^a,c  

^a University of Washington   (United States)

^b SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Calvarial osteoblast; Cell migration; IGF1; IGF1R; Single suture craniosynostosis; Traction force

Indexed keywords

BIOLOGICAL MARKER; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; IGF1 PROTEIN, HUMAN;

ARTICLE; CALVARIA; CELL MIGRATION; CELL MOTILITY; CONTROLLED STUDY; CRANIOFACIAL SYNOSTOSIS; GENOTYPE PHENOTYPE CORRELATION; HUMAN; HUMAN CELL; OSTEOBLAST; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TIME-LAPSE VIDEO MICROSCOPY; TRANSCRIPTOMICS; UPREGULATION; CELL ADHESION; CELL CULTURE; CELL MOTION; METABOLISM; PHYSIOLOGY;

CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; HUMANS; INSULIN-LIKE GROWTH FACTOR I; OSTEOBLASTS; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION;

EID: 84957685602     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.175976     Document Type: Article

References (86)

1. Al-Rekabi, Z. and Pelling, A. E. (2013). Cross talk between matrix elasticity and mechanical force regulates myoblast traction dynamics. Phys. Biol. 10, 066003.
2. Andersson, S., D'Arcy, P., Larsson, O. and Sehat, B. (2009). Focal adhesion kinase (FAK) activates and stabilizes IGF-1 receptor. Biochem. Biophys. Res. Commun. 387, 36-41.
3. Andrade, A. C., Nilsson, O., Barnes, K. M. and Baron, J. (2007). Wnt gene expression in the post-natal growth plate: regulation with chondrocyte differentiation. Bone 40, 1361-1369.
4. Baker, J., Liu, J.-P., Robertson, E. J. and Efstratiadis, A. (1993). Role of insulinlike growth factors in embryonic and postnatal growth. Cell 75, 73-82.
5. Behr, B., Longaker, M. T. and Quarto, N. (2010). Differential activation of canonical Wnt signaling determines cranial sutures fate: a novel mechanism for sagittal suture craniosynostosis. Dev. Biol. 344, 922-940.
6. Beningo, K. A., Hamao, K., Dembo, M., Wang, Y.-L. and Hosoya, H. (2006). Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase. Arch. Biochem. Biophys. 456, 224-231.
7. Bikle, D., Majumdar, S., Laib, A., Powell-Braxton, L., Rosen, C., Beamer, W., Nauman, E., Leary, C. and Halloran, B. (2001). The skeletal structure of insulinlike growth factor I-deficient mice. J. Bone Miner. Res. 16, 2320-2329.
8. Bodine, P. V. N., Seestaller-Wehr, L., Kharode, Y. P., Bex, F. J. and Komm, B. S. (2007). Bone anabolic effects of parathyroid hormone are blunted by deletion of the Wnt antagonist secreted frizzled-related protein-1. J. Cell. Physiol. 210, 352-357.
9. Bradley, J. P., Han, V. K. M., Roth, D. A., Levine, J. P., McCarthy, J. G. and Longaker, M. T. (1999). Increased IGF-I and IGF-II mRNA and IGF-I peptide in fusing rat cranial sutures suggest evidence for a paracrine role of insulin-like growth factors in suture fusion. Plast. Reconstr. Surg. 104, 129-138.
10. Brunner, M., Millon-Fremillon, A., Chevalier, G., Nakchbandi, I. A., Mosher, D., Block, M. R., Albiges-Rizo, C. and Bouvard, D. (2011). Osteoblast mineralization requires beta1 integrin/ICAP-1-dependent fibronectin deposition. J. Cell Biol. 194, 307-322.
11. Buxboim, A., Rajagopal, K., Brown, A. E. X. and Discher, D. E. (2010). How deeply cells feel: methods for thin gels. J. Phys. Condens. Matter 22, 194116.
12. Carmichael, S. L., Clarke, C. M. and Cunningham, M. L. (2015a). Craniosynostosis: the potential contribution of thyroid-related mechanisms. Curr. Epidemiol. Rep. 2, 1-7.
13. Carmichael, S. L., Ma, C., Rasmussen, S. A., Cunningham, M. L., Browne, M. L., Dosiou, C., Lammer, E. J. and Shaw, G. M. (2015b). Craniosynostosis and risk factors related to thyroid dysfunction. Am. J. Med. Genet. A 167, 701-707.
14. Chen, C. S. (2008). Mechanotransduction-a field pulling together? J. Cell Sci. 121, 3285-3292.
15. Chen, Y., Zhang, D. S., Tao, P. Y., Xu, P., Feng, S. Z., Mu, X. Z. and Wei, M. (2003). The effect of insulin-like growth factor 1 on the fusion of cranial suture. Zhonghua Zheng Xing Wai Ke Za Zhi 19, 11-14.
16. Chrzanowska-Wodnicka, M. and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
17. Coussens, A. K., Hughes, I. P., Wilkinson, C. R., Morris, C. P., Anderson, P. J., Powell, B. C. and van Daal, A. (2008). Identification of genes differentially expressed by prematurely fused human sutures using a novel in vivo-in vitro approach. Differentiation 76, 531-545.
18. Cunningham, M. L., Horst, J. A., Rieder, M. J., Hing, A. V., Stanaway, I. B., Park, S. S., Samudrala, R. and Speltz, M. L. (2011). IGF1R variants associated with isolated single suture craniosynostosis. Am. J. Med. Genet. A 155, 91-97.
19. Cvetkovic, C., Raman, R., Chan, V., Williams, B. J., Tolish, M., Bajaj, P., Sakar, M. S., Asada, H. H., Saif, M. T. A. and Bashir, R. (2014). Three-dimensionally printed biological machines powered by skeletal muscle. Proc. Natl. Acad. Sci. USA 111, 10125-10130.
20. Doerr, M. E. and Jones, J. I. (1996). The roles of integrins and extracellular matrix proteins in the insulin-like growth factor I-stimulated chemotaxis of human breast cancer cells. J. Biol. Chem. 271, 2443-2447.
21. Engler, A. J., Sen, S., Sweeney, H. L. and Discher, D. E. (2006). Matrix elasticity directs stem cell lineage specification. Cell 126, 677-689.
22. Fanganiello, R. D., Sertie, A. L., Reis, E. M., Yeh, E., Oliveira, N. A., Bueno, D. F., Kerkis, I., Alonso, N., Cavalheiro, S., Matsushita, H. et al. (2007). Apert p. Ser252Trp mutation in FGFR2 alters osteogenic potential and gene expression of cranial periosteal cells. Mol. Med. 13, 422-442.
23. Fitzpatrick, D. R. (2013). Filling in the gaps in cranial suture biology. Nat. Genet. 45, 231-232.
24. Fukata, Y., Kaibuchi, K., Amano, M. and Kaibuchi, K. (2001). Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of nonmuscle cells. Trends Pharmacol. Sci. 22, 32-39.
25. Gardel, M. L., Sabass, B., Ji, L., Danuser, G., Schwarz, U. S. and Waterman, C. M. (2008). Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 183, 999-1005.
26. Gawlitta, D., Boonen, K. J. M., Oomens, C. W. J., Baaijens, F. P. T. and Bouten, C. V. C. (2008). The influence of serum-free culture conditions on skeletal muscle differentiation in a tissue-engineered model. Tissue Eng. A 14, 161-171.
27. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J. et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
28. Graham, J. M., Jr and Smith, D. W. (1980). Metopic craniostenosis as a consequence of fetal head constraint: two interesting experiments of nature. Pediatrics 65, 1000-1002.
29. Graham, J. M., Jr, De Saxe, M. and Smith, D. W. (1979). Sagittal craniostenosis: fetal head constraint as one possible cause. J. Pediatr. 95, 747-750.
30. Graham, J. M., Jr, Badura, R. J. and Smith, D. W. (1980). Coronal craniostenosis: fetal head constraint as one possible cause. Pediatrics 65, 995-999.
31. Gross, T. S., Srinivasan, S., Liu, C. C., Clemens, T. L. and Bain, S. D. (2002). Noninvasive loading of the murine tibia: an in vivo model for the study of mechanotransduction. J. Bone Miner. Res. 17, 493-501.
32. Guntur, A. R. and Rosen, C. J. (2013). IGF-1 regulation of key signaling pathways in bone. BoneKEy Rep. 2, 437.
33. Guvakova, M. A. (2007). Insulin-like growth factors control cell migration in health and disease. Int. J. Biochem. Cell Biol. 39, 890-909.
34. Haase, I., Evans, R., Pofahl, R. and Watt, F. M. (2003). Regulation of keratinocyte shape, migration and wound epithelialization by IGF-1-and EGF-dependent signalling pathways. J. Cell Sci. 116, 3227-3238.
35. Hall, B. K. and Miyake, T. (2000). All for one and one for all: condensations and the initiation of skeletal development. BioEssays 22, 138-147.
36. Han, S. J., Bielawski, K. S., Ting, L. H., Rodriguez, M. L. and Sniadecki, N. J. (2012). Decoupling substrate stiffness, spread area, and micropost density: a close spatial relationship between traction forces and focal adhesions. Biophys. J. 103, 640-648.
37. Hirukawa, K., Miyazawa, K., Maeda, H., Kameyama, Y., Goto, S. and Togari, A. (2005). Effect of tensile force on the expression of IGF-I and IGF-I receptor in the organ-cultured rat cranial suture. Arch. Oral Biol. 50, 367-372.
38. Honein, M. A. and Rasmussen, S. A. (2000). Further evidence for an association between maternal smoking and craniosynostosis. Teratology 62, 145-146.
39. Hunter, C., Bond, J., Kuo, P. C., Selim, M. A. and Levinson, H. (2012). The role of osteopontin and osteopontin aptamer (OPN-R3) in fibroblast activity. J. Surg. Res. 176, 348-358.
40. Ingber, D. E. (2006). Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20, 811-827.
41. Jaalouk, D. E. and Lammerding, J. (2009). Mechanotransduction gone awry. Nat. Rev. Mol. Cell Biol. 10, 63-73.
42. James, A.W., Theologis, A. A., Brugmann, S. A., Xu, Y., Carre, A. L., Leucht, P., Hamilton, K., Korach, K. S. and Longaker, M. T. (2009). Estrogen/estrogen receptor alpha signaling in mouse posterofrontal cranial suture fusion. PLoS ONE 4, e7120.
43. Jiang, Z., Von den Hoff, J.W., Torensma, R., Meng, L. and Bian, Z. (2014). Wnt16 is involved in intramembranous ossification and suppresses osteoblast differentiation through the Wnt/beta-catenin pathway. J. Cell. Physiol. 229, 384-392.
44. Kallen, K. (1999). Maternal smoking and craniosynostosis. Teratology 60, 146-150.
45. Kilian, K. A., Bugarija, B., Lahn, B. T. and Mrksich, M. (2010). Geometric cues for directing the differentiation of mesenchymal stem cells. Proc. Natl. Acad. Sci. USA 107, 4872-4877.
46. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R. and Salzberg, S. L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.
47. Kim, D.-H., Cho, S. and Wirtz, D. (2014). Tight coupling between nucleus and cell migration through the perinuclear actin cap. J. Cell Sci. 127, 2528-2541.
48. Klein-Nulend, J., Bakker, A. D., Bacabac, R. G., Vatsa, A. and Weinbaum, S. (2013). Mechanosensation and transduction in osteocytes. Bone 54, 182-190.
49. Kurokawa, K. and Matsuda, M. (2005). Localized RhoA activation as a requirement for the induction of membrane ruffling. Mol. Biol. Cell 16, 4294-4303.
50. Laviola, L., Natalicchio, A. and Giorgino, F. (2007). The IGF-I signaling pathway. Curr. Pharm. Des. 13, 663-669.
51. Lemonnier, J., Haÿ, E., Delannoy, P., Lomri, A., Modrowski, D., Caverzasio, J. and Marie, P. J. (2001). Role of N-cadherin and protein kinase C in osteoblast gene activation induced by the S252Wfibroblast growth factor receptor 2 mutation in Apert craniosynostosis. J. Bone Miner. Res. 16, 832-845.
52. Liaw, L., Almeida, M., Hart, C. E., Schwartz, S. M. and Giachelli, C. M. (1994). Osteopontin promotes vascular cell adhesion and spreading and is chemotactic for smooth muscle cells in vitro. Circ. Res. 74, 214-224.
53. Lin, I. C., Slemp, A. E., Hwang, C., Sena-Esteves, M., Nah, H.-D. and Kirschner, R. E. (2007). Dihydrotestosterone stimulates proliferation and differentiation of fetal calvarial osteoblasts and dural cells and induces cranial suture fusion. Plast. Reconstr. Surg. 120, 1137-1147.
54. Liu, J.-P., Baker, J., Perkins, A. S., Robertson, E. J. and Efstratiadis, A. (1993). Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75, 59-72.
55. Lomri, A., Lemonnier, J., Hott, M., de Parseval, N., Lajeunie, E., Munnich, A., Renier, D. and Marie, P. J. (1998). Increased calvaria cell differentiation and bone matrix formation induced by fibroblast growth factor receptor 2 mutations in Apert syndrome. J. Clin. Invest. 101, 1310-1317.
56. Lories, R. J., Corr, M. and Lane, N. E. (2013). To Wnt or not to Wnt: the bone and joint health dilemma. Nat. Rev. Rheumatol. 9, 328-339.
57. Manes, S., Mira, E., Gomez-Mouton, C., Zhao, Z. J., Lacalle, R. A. and Martinez-A, C. (1999). Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol. Cell. Biol. 19, 3125-3135.
58. Maruyama, T., Mirando, A. J., Deng, C. X. and Hsu, W. (2010). The balance of WNT and FGF signaling influences mesenchymal stem cell fate during skeletal development. Sci. Signal. 3, ra40.
59. McBeath, R., Pirone, D. M., Nelson, C. M., Bhadriraju, K. and Chen, C. S. (2004). Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483-495.
60. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M. et al. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.
61. Miraoui, H., Ringe, J., Haupl, T. and Marie, P. J. (2010). Increased EFG-and PDGFalpha-receptor signaling by mutant FGF-receptor 2 contributes to osteoblast dysfunction in Apert craniosynostosis. Hum. Mol. Gen. 19, 1678-1689.
62. Mukherjee, S. and Guidry, C. (2007). The insulin-like growth factor system modulates retinal pigment epithelial cell tractional force generation. Invest. Ophthalmol. Vis. Sci. 48, 1892-1899.
63. Olsen, B. R., Reginato, A. M. and Wang, W. (2000). Bone development. Annu. Rev. Cell Dev. Biol. 16, 191-220.
64. Park, S. S., Beyer, R. P., Smyth, M. D., Clarke, C. M., Timms, A. E., Bammler, T. K., Stamper, B. D., Mecham, B. H., Gustafson, J. A. and Cunningham, M. L. (2015). Osteoblast differentiation profiles define sex specific gene expression patterns in craniosynostosis. Bone 76, 169-176.
65. Passos-Bueno, M. R., Serti Eacute, A. E., Jehee, F. S., Fanganiello, R. and Yeh, E. (2008). Genetics of craniosynostosis: genes, syndromes, mutations and genotype-phenotype correlations. Front. Oral Biol. 12, 107-143.
66. Rasmussen, S. A., Yazdy, M. M., Carmichael, S. L., Jamieson, D. J., Canfield, M. A. and Honein, M. A. (2007). Maternal thyroid disease as a risk factor for craniosynostosis. Obstet. Gynecol. 110, 369-377.
67. Rath, B., Nam, J., Knobloch, T. J., Lannutti, J. J. and Agarwal, S. (2008). Compressive forces induce osteogenic gene expression in calvarial osteoblasts. J. Biomech. 41, 1095-1103.
68. Reefhuis, J., Honein, M. A., Shaw, G. M. and Romitti, P. A. (2003). Fertility treatments and craniosynostosis: California, Georgia, and Iowa, 1993-1997. Pediatrics 111, 1163-1166.
69. Reijnders, C. M. A., Bravenboer, N., Tromp, A. M., Blankenstein, M. A. and Lips, P. (2007). Effect of mechanical loading on insulin-like growth factor-I gene expression in rat tibia. J. Endocrinol. 192, 131-140.
70. Roth, D. A., Gold, L. I., Han, V. K. M., McCarthy, J. G., Sung, J. J., Wisoff, J. H. and Longaker, M. T. (1997). Immunolocalization of transforming growth factor beta 1, beta 2, and beta 3 and insulin-like growth factor I in premature cranial suture fusion. Plast. Reconstr. Surg. 99, 300-309; discussion 310-306.
71. Schoen, I., Hu, W., Klotzsch, E. and Vogel, V. (2010). Probing cellular traction forces by micropillar arrays: contribution of substrate warping to pillar deflection. Nano Lett. 10, 1823-1830.
72. Sharma, V. P., Fenwick, A. L., Brockop, M. S., McGowan, S. J., Goos, J. A. C., Hoogeboom, A. J. M., Brady, A. F., Jeelani, N. O., Lynch, S. A., Mulliken, J. B. et al. (2013). Mutations in TCF12, encoding a basic helix-loop-helix partner of TWIST1, are a frequent cause of coronal craniosynostosis. Nat. Genet. 45, 304-307.
73. Sniadecki, N. J. and Chen, C. S. (2007). Microfabricated silicone elastomeric post arrays for measuring traction forces of adherent cells. Methods Cell Biol. 83, 313-328.
74. Sniadecki, N. J., Anguelouch, A., Yang, M. T., Lamb, C. M., Liu, Z., Kirschner, S. B., Liu, Y., Reich, D. H. and Chen, C. S. (2007). Magnetic microposts as an approach to apply forces to living cells. Proc. Natl. Acad. Sci. USA 104, 14553-14558.
75. Stamper, B. D., Park, S. S., Beyer, R. P., Bammler, T. K., Farin, F. M., Mecham, B. and Cunningham, M. L. (2011). Differential expression of extracellular matrixmediated pathways in single-suture craniosynostosis. PLoS ONE 6, e26557.
76. Stamper, B. D., Mecham, B., Park, S. S., Wilkerson, H., Farin, F. M., Beyer, R. P., Bammler, T. K., Mangravite, L. M. and Cunningham, M. L. (2012). Transcriptome correlation analysis identifies two unique craniosynostosis subtypes associated with IRS1 activation. Physiol. Genomics 44, 1154-1163.
77. Tahimic, C. G. T., Wang, Y. and Bikle, D. D. (2013). Anabolic effects of IGF-1 signaling on the skeleton. Front. Endocrinol. 4, 6.
78. Taya, S., Inagaki, N., Sengiku, H., Makino, H., Iwamatsu, A., Urakawa, I., Nagao, K., Kataoka, S. and Kaibuchi, K. (2001). Direct interaction of insulin-like growth factor-1 receptor with leukemia-associated RhoGEF. J. Cell Biol. 155, 809-820.
79. ten Berge, D., Brugmann, S. A., Helms, J. A. and Nusse, R. (2008). Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development. Development 135, 3247-3257.
80. Ting, M.-C., Wu, N. L., Roybal, P. G., Sun, J., Liu, L., Yen, Y. and Maxson, R. E., Jr (2009). EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis. Development 136, 855-864.
81. Twigg, S. R. F. and Wilkie, A. O. M. (2015). A genetic-pathophysiological framework for craniosynostosis. Am. J. Hum. Genet. 97, 359-377.
82. Twigg, S. R. F., Vorgia, E., McGowan, S. J., Peraki, I., Fenwick, A. L., Sharma, V. P., Allegra, M., Zaragkoulias, A., Sadighi Akha, E., Knight, S. J. L. et al. (2013). Reduced dosage of ERF causes complex craniosynostosis in humans and mice and links ERK1/2 signaling to regulation of osteogenesis. Nat. Genet. 45, 308-313.
83. Vandenburgh, H., Shansky, J., Benesch-Lee, F., Barbata, V., Reid, J., Thorrez, L., Valentini, R. and Crawford, G. (2008). Drug-screening platform based on the contractility of tissue-engineered muscle. Muscle Nerve 37, 438-447.
84. Wang, Y.-K., Yu, X., Cohen, D. M., Wozniak, M. A., Yang, M. T., Gao, L., Eyckmans, J. and Chen, C. S. (2012). Bone morphogenetic protein-2-induced signaling and osteogenesis is regulated by cell shape, RhoA/ROCK, and cytoskeletal tension. Stem Cells Dev. 21, 1176-1186.
85. Woods, K. A., Camacho-Hübner, C., Savage, M. O. and Clark, A. J. L. (1996). Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N. Engl. J. Med. 335, 1363-1367.
86. Yen, H.-Y., Ting, M.-C. and Maxson, R. E. (2010). Jagged1 functions downstream of Twist1 in the specification of the coronal suture and the formation of a boundary between osteogenic and non-osteogenic cells. Dev. Biol. 347, 258-270.