Tissue stiffness regulates serine/arginine-rich protein-mediated splicing of the extra domain B-fibronectin isoform in tumors

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

Volumn 112, Issue 27, 2015, Pages 8314-8319

  Bordeleau, Francois ^a   Califano, Joseph P ^a   Abril, Yashira L Negrón ^b   Mason, Brooke N ^a   LaValley, Danielle J ^a   Shin, Sandra J ^c   Weiss, Robert S ^b   Reinhart King, Cynthia A ^a   Anseth, Kristi S ^d  

^a School of Operations Research and Industrial Engineering   (United States)

^b New York Presbyterian Hospital Weill ^*  (United States)

^c NEW YORK PRESBYTERIAN HOSPITAL   (United States)

^d UNIVERSITY OF COLORADO   (United States)

Author keywords

Alternative splicing; Angiogenesis; Cancer progression; Extracellular matrix; Matrix stiffness

Indexed keywords

FIBRONECTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C BETA; SERINE ARGININE RICH PROTEIN; VASCULOTROPIN; ARGININE; ISOPROTEIN; RHO KINASE; SERINE; VASCULOTROPIN A;

ALTERNATIVE RNA SPLICING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST TUMOR; CARCINOGENESIS; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; TUMOR MICROENVIRONMENT; TUMOR VASCULARIZATION; ANIMAL; BINDING SITE; BIOMECHANICS; BOVINE; CELL CULTURE; CHEMISTRY; CONFOCAL MICROSCOPY; GENETICS; METABOLISM; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); RNA INTERFERENCE; SIGNAL TRANSDUCTION; VASCULARIZATION; WESTERN BLOTTING;

MURINAE;

ALTERNATIVE SPLICING; ANIMALS; ARGININE; BINDING SITES; BIOMECHANICAL PHENOMENA; BLOTTING, WESTERN; CATTLE; CELLS, CULTURED; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FIBRONECTINS; HUMANS; MICE; MICROSCOPY, CONFOCAL; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-AKT; RHO-ASSOCIATED KINASES; RNA INTERFERENCE; SERINE; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84936817685     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505421112     Document Type: Article

References (68)

1. Ghigna C, Valacca C, Biamonti G (2008) Alternative splicing and tumor progression. Curr Genomics 9(8):556-570.
2. Oltean S, Bates DO (2014) Hallmarks of alternative splicing in cancer. Oncogene 33(46):5311-5318.
3. Irimia M, Blencowe BJ (2012) Alternative splicing: Decoding an expansive regulatory layer. Curr Opin Cell Biol 24(3):323-332.
4. Brinkman BM (2004) Splice variants as cancer biomarkers. Clin Biochem 37(7): 584-594.
5. Long JC, Caceres JF (2009) The SR protein family of splicing factors: Master regulators of gene expression. Biochem J 417(1):15-27.
6. Neri D, Bicknell R (2005) Tumour vascular targeting. Nat Rev Cancer 5(6):436-446.
7. Castellani P, et al. (2002) Differentiation between high- and low-grade astrocytoma using a human recombinant antibody to the extra domain-B of fibronectin. Am J Pathol 161(5):1695-1700.
8. Zardi L, et al. (1987) Transformed human cells produce a new fibronectin isoform by preferential alternative splicing of a previously unobserved exon. EMBO J 6(8):2337-2342.
9. Khan ZA, et al. (2005) EDB fibronectin and angiogenesis-A novel mechanistic pathway. Angiogenesis 8(3):183-196.
10. Lim LP, Sharp PA (1998) Alternative splicing of the fibronectin EIIIB exon depends on specific TGCATG repeats. Mol Cell Biol 18(7):3900-3906.
11. Han F, et al. (2007) Transforming growth factor-beta1 regulates fibronectin isoform expression and splicing factor SRp40 expression during ATDC5 chondrogenic maturation. Exp Cell Res 313(8):1518-1532.
12. Du K, Peng Y, Greenbaum LE, Haber BA, Taub R (1997) HRS/SRp40-mediated inclusion of the fibronectin EIIIB exon, a possible cause of increased EIIIB expression in proliferating liver. Mol Cell Biol 17(7):4096-4104.
13. Saitoh N, et al. (2012) The distribution of phosphorylated SR proteins and alternative splicing are regulated by RANBP2. Mol Biol Cell 23(6):1115-1128.
14. Patel NA, et al. (2005) Molecular and genetic studies imply Akt-mediated signaling promotes protein kinase CbetaII alternative splicing via phosphorylation of serine/arginine-rich splicing factor SRp40. J Biol Chem 280(14):14302-14309.
15. Prasad J, Colwill K, Pawson T, Manley JL (1999) The protein kinase Clk/Sty directly modulates SR protein activity: Both hyper- and hypophosphorylation inhibit splicing. Mol Cell Biol 19(10):6991-7000.
16. Patel NA, et al. (2001) Insulin regulates alternative splicing of protein kinase C beta II through a phosphatidylinositol 3-kinase-dependent pathway involving the nuclear serine/arginine-rich splicing factor, SRp40, in skeletal muscle cells. J Biol Chem 276(25): 22648-22654.
17. Mouw JK, et al. (2014) Tissue mechanics modulate microRNA-dependent PTEN expression to regulate malignant progression. Nat Med 20(4):360-367.
18. Leight JL, Wozniak MA, Chen S, Lynch ML, Chen CS (2012) Matrix rigidity regulates a switch between TGF-β1-induced apoptosis and epithelial-mesenchymal transition. Mol Biol Cell 23(5):781-791.
19. Schrader J, et al. (2011) Matrix stiffness modulates proliferation, chemotherapeutic response, and dormancy in hepatocellular carcinoma cells. Hepatology 53(4):1192-1205.
20. Levental KR, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139(5):891-906.
21. DuFort CC, Paszek MJ, Weaver VM (2011) Balancing forces: Architectural control of mechanotransduction. Nat Rev Mol Cell Biol 12(5):308-319.
22. Kim JH, Asthagiri AR (2011) Matrix stiffening sensitizes epithelial cells to EGF and enables the loss of contact inhibition of proliferation. J Cell Sci 124(Pt 8):1280-1287.
23. Plodinec M, et al. (2012) The nanomechanical signature of breast cancer. Nat Nanotechnol 7(11):757-765.
24. Pathak A, Kumar S (2013) Transforming potential and matrix stiffness co-regulate confinement sensitivity of tumor cell migration. Integr Biol (Camb) 5(8):1067-1075.
25. Bordeleau F, Alcoser TA, Reinhart-King CA (2014) Physical biology in cancer. 5. The rocky road of metastasis: The role of cytoskeletal mechanics in cell migratory response to 3D matrix topography. Am J Physiol Cell Physiol 306(2):C110-C120.
26. Peyton SR, Putnam AJ (2005) Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J Cell Physiol 204(1):198-209.
27. Paszek MJ, et al. (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241-254.
28. Carraher CL, Schwarzbauer JE (2013) Regulation of matrix assembly through rigiditydependent fibronectin conformational changes. J Biol Chem 288(21):14805-14814.
29. Kubow KE, et al. (2009) Crosslinking of cell-derived 3D scaffolds up-regulates the stretching and unfolding of new extracellular matrix assembled by reseeded cells. Integr Biol (Camb) 1(11-12):635-648.
30. Kim J, et al. (2008) Centrosomal PKCbetaII and pericentrin are critical for human prostate cancer growth and angiogenesis. Cancer Res 68(16):6831-6839.
31. Nowak DG, et al. (2010) Regulation of vascular endothelial growth factor (VEGF) splicing from pro-angiogenic to anti-angiogenic isoforms: A novel therapeutic strategy for angiogenesis. J Biol Chem 285(8):5532-5540.
32. Huynh J, Bordeleau F, Kraning-Rush CM, Reinhart-King CA (2013) Substrate stiffness regulates PDGF-induced circular dorsal ruffle formation through MLCK. Cell Mol Bioeng 6(2):138-147.
33. Meyer-ter-Vehn T, et al. (2006) Contractility as a prerequisite for TGF-beta-induced myofibroblast transdifferentiation in human tenon fibroblasts. Invest Ophthalmol Vis Sci 47(11):4895-4904.
34. Helfman DM, Pawlak G (2005) Myosin light chain kinase and acto-myosin contractility modulate activation of the ERK cascade downstream of oncogenic Ras. J Cell Biochem 95(5):1069-1080.
35. Phanish MK, et al. (2014) The regulation of TGFβ1 induced fibronectin EDA exon alternative splicing in human renal proximal tubule epithelial cells [published online ahead of print June 24, 2014]. J Cell Physiol, 10.1002/jcp.24703.
36. Astrof S, et al. (2004) Direct test of potential roles of EIIIA and EIIIB alternatively spliced segments of fibronectin in physiological and tumor angiogenesis. Mol Cell Biol 24(19):8662-8670.
37. Coltrini D, et al. (2009) Impact of VEGF-dependent tumour micro-environment on EDB fibronectin expression by subcutaneous human tumour xenografts in nude mice. J Pathol 219(4):455-462.
38. Hashimoto-Uoshima M, Yan YZ, Schneider G, Aukhil I (1997) The alternatively spliced domains EIIIB and EIIIA of human fibronectin affect cell adhesion and spreading. J Cell Sci 110(Pt 18):2271-2280.
39. White ES, Muro AF (2011) Fibronectin splice variants: Understanding their multiple roles in health and disease using engineered mouse models. IUBMB Life 63(7):538-546.
40. Nowak DG, et al. (2008) Expression of pro- and anti-angiogenic isoforms of VEGF is differentially regulated by splicing and growth factors. J Cell Sci 121(Pt 20):3487-3495.
41. Cooper DR, et al. (2014) Long non-coding RNA NEAT1 associates with SRp40 to temporally regulate PPARγ2 splicing during adipogenesis in 3T3-L1 cells. Genes (Basel) 5(4): 1050-1063.
42. Wee CD, Havens MA, Jodelka FM, Hastings ML (2014) Targeting SR proteins improves SMN expression in spinal muscular atrophy cells. PLoS ONE 9(12):e115205.
43. Yan XB, et al. (2010) Alternative splicing in exon 9 of glucocorticoid receptor premRNA is regulated by SRp40. Mol Biol Rep 37(3):1427-1433.
44. Umesh V, Rape AD, Ulrich TA, Kumar S (2014) Microenvironmental stiffness enhances glioma cell proliferation by stimulating epidermal growth factor receptor signaling. PLoS ONE 9(7):e101771.
45. Scarpino S, et al. (1999) Expression of EDA/EDB isoforms of fibronectin in papillary carcinoma of the thyroid. J Pathol 188(2):163-167.
46. Hauptmann S, et al. (1995) Extracellular matrix proteins in colorectal carcinomas. Expression of tenascin and fibronectin isoforms. Lab Invest 73(2):172-182.
47. Castellani P, et al. (1994) The fibronectin isoform containing the ED-B oncofetal domain: A marker of angiogenesis. Int J Cancer 59(5):612-618.
48. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: The next generation. Cell 144(5):646-674.
49. Dales JP, et al. (2010) Hypoxia inducible factor 1alpha gene (HIF-1alpha) splice variants: Potential prognostic biomarkers in breast cancer. BMC Med 8:44.
50. Vogel V, Sheetz MP (2009) Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr Opin Cell Biol 21(1):38-46.
51. Zeng Y, Lai T, Koh CG, LeDuc PR, Chiam KH (2011) Investigating circular dorsal ruffles through varying substrate stiffness and mathematical modeling. Biophys J 101(9): 2122-2130.
52. Bordeleau F, Galarneau L, Gilbert S, Loranger A, Marceau N (2010) Keratin 8/18 modulation of protein kinase C-mediated integrin-dependent adhesion and migration of liver epithelial cells. Mol Biol Cell 21(10):1698-1713.
53. Larsson C (2006) Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal 18(3):276-284.
54. Ng T, et al. (1999) PKCalpha regulates beta1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J 18(14):3909-3923.
55. Oh MA, et al. (2007) PKCdelta and cofilin activation affects peripheral actin reorganization and cell-cell contact in cells expressing integrin alpha5 but not its tailless mutant. J Cell Sci 120(Pt 15):2717-2730.
56. Zhao W, Li X, Liu X, Zhang N, Wen X (2014) Effects of substrate stiffness on adipogenic and osteogenic differentiation of human mesenchymal stem cells. Mater Sci Eng C Mater Biol Appl 40:316-323.
57. Lopez JI, Kang I, You WK, McDonald DM, Weaver VM (2011) In situ force mapping of mammary gland transformation. Integr Biol (Camb) 3(9):910-921.
58. Chang SC, et al. (2001) Injection molding of chondrocyte/alginate constructs in the shape of facial implants. J Biomed Mater Res 55(4):503-511.
59. Gleghorn JP, Jones AR, Flannery CR, Bonassar LJ (2007) Boundary mode frictional properties of engineered cartilaginous tissues. Eur CellMater 14:20-28, discussion 28-29.
60. Bonnevie ED, Puetzer JL, Bonassar LJ (2014) Enhanced boundary lubrication properties of engineered menisci by lubricin localization with insulin-like growth factor I treatment. J Biomech 47(9):2183-2188.
61. Califano JP, Reinhart-King CA (2010) Substrate stiffness and cell area drive cellular traction stresses in single cells and cells in contact. Cell Mol Bioeng 3(1):68-75.
62. Kraning-Rush CM, Califano JP, Reinhart-King CA (2012) Cellular traction stresses increase with increasing metastatic potential. PLoS ONE 7(2):e32572.
63. Califano JP, Reinhart-King CA (2008) A balance of substrate mechanics and matrix chemistry regulates endothelial cell network assembly. Cell Molec Bioengineer 1(2-3): 122-132.
64. Reinhart-King CA, Dembo M, Hammer DA (2003) Endothelial cell traction forces on RGD-derivatized polyacrylamide substrata. Langmuir 19(5):1573-1579.
65. Huynh J, et al. (2011) Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration. Sci Transl Med 3(112):112ra122.
66. Peloquin J, Huynh J, Williams RM, Reinhart-King CA (2011) Indentation measurements of the subendothelial matrix in bovine carotid arteries. J Biomech 44(5): 815-821.
67. Bordeleau F, Myrand Lapierre M-E, Sheng Y, Marceau N (2012) Keratin 8/18 regulation of cell stiffness-extracellular matrix interplay through modulation of Rho-mediated actin cytoskeleton dynamics. PLoS ONE 7(6):e38780.
68. Cseh B, et al. (2010) Autocrine fibronectin directs matrix assembly and crosstalk between cell-matrix and cell-cell adhesion in vascular endothelial cells. J Cell Sci 123(Pt 22): 3989-3999.