Shp2 plays a crucial role in cell structural orientation and force polarity in response to matrix rigidity

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

Volumn 110, Issue 8, 2013, Pages 2840-2845

  Lee, Hsiao Hui ^a   Lee, Hsin Chang ^a   Chou, Chih Chiang ^a   Hur, Sung Sik ^b,c   Osterday, Katie ^c,d   Del Álamo, Juan C ^c,d   Lasheras, Juan C ^b,c,d   Chien, Shu ^b,c  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytoskeletal architecture; Mechanosensing; Mechanotransduction; Phosphorylation

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; FLUORESCEIN ISOTHIOCYANATE; PAXILLIN; PHALLOIDIN; PROTEIN TYROSINE PHOSPHATASE SHP 2;

ANIMAL CELL; ARTICLE; CELL ELONGATION; CELL FUNCTION; CELL MATURATION; CELL POLARITY; CELL SHAPE; CELL SPREADING; CELL STRUCTURE; CYTOSKELETON; EMBRYO; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; IMMUNOFLUORESCENCE; MECHANICAL STRESS; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RIGIDITY; STRESS FIBER; WESTERN BLOTTING;

ANIMALS; CELL MOVEMENT; CELL SHAPE; CELLS, CULTURED; EXTRACELLULAR MATRIX; FOCAL ADHESIONS; MICE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 11;

EID: 84874222503     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1222164110     Document Type: Article

References (58)

1. Mammoto A, Ingber DE (2009) Cytoskeletal control of growth and cell fate switching. Curr Opin Cell Biol 21 (6):864-870.
2. Engler AJ, Sen S, Sweeney HL, Discher DE (2006) Matrix elasticity directs stem cell lineage specification. Cell 126 (4):677-689.
3. Levental KR, et al. (2009) Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139 (5):891-906.
4. Discher DE, Janmey P, Wang YL (2005) Tissue cells feel and respond to the stiffness of their substrate. Science 310 (5751):1139-1143.
5. Wang N, Tytell JD, Ingber DE (2009) Mechanotransduction at a distance: Mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10 (1):75-82.
6. Jaalouk DE, Lammerding J (2009) Mechanotransduction gone awry. Nat Rev Mol Cell Biol 10 (1):63-73.
7. Ingber DE (1997) Integrins, tensegrity, and mechanotransduction. Gravit Space Biol Bull 10 (2):49-55.
8. Chowdhury F, et al. (2010) Material properties of the cell dictate stress-induced spreading and differentiation in embryonic stem cells. Nat Mater 9 (1):82-88.
9. Wozniak MA, Chen CS (2009) Mechanotransduction in development: A growing role for contractility. Nat Rev Mol Cell Biol 10 (1):34-43.
10. Kolahi KS, Mofrad MR (2010) Mechanotransduction: A major regulator of homeostasis and development. Wiley Interdiscip Rev Syst Biol Med 2 (6):625-639.
11. Schwartz MA, DeSimone DW (2008) Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 20 (5):551-556.
12. Geiger B, Spatz JP, Bershadsky AD (2009) Environmental sensing through focal adhesions. Nat Rev Mol Cell Biol 10 (1):21-33.
13. Harburger DS, Calderwood DA (2009) Integrin signalling at a glance. J Cell Sci 122 (Pt 2):159-163.
14. Zhang X, et al. (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat Cell Biol 10 (9):1062-1068.
15. del Rio A, et al. (2009) Stretching single talin rod molecules activates vinculin binding. Science 323 (5914):638-641.
16. Parsons JT, Horwitz AR, Schwartz MA (2010) Cell adhesion: Integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11 (9):633-643.
17. Webb DJ, Parsons JT, Horwitz AF (2002) Adhesion assembly, disassembly and turnover in migrating cells-over and over and over again. Nat Cell Biol 4 (4):E97-E100.
18. Huveneers S, Danen EH (2009) Adhesion signaling: Crosstalk between integrins, Src and Rho. J Cell Sci 122 (Pt 8):1059-1069.
19. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B (2007) Functional atlas of the integrin adhesome. Nat Cell Biol 9 (8):858-867.
20. Kaazempur Mofrad MR, et al. (2005) Exploring the molecular basis for mechano-sensation, signal transduction, and cytoskeletal remodeling. Acta Biomater 1 (3):281-293.
21. Ingber DE (2003) Mechanobiology and diseases of mechanotransduction. Ann Med35 (8):564-577.
22. Neel BG, Gu H, Pao L (2003) The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem Sci 28 (6):284-293.
23. Grossmann KS, Rosário M, Birchmeier C, Birchmeier W (2010) The tyrosine phosphatase Shp2 in development and cancer. Adv Cancer Res 106:53-89.
24. Chan G, Kalaitzidis D, Neel BG (2008) The tyrosine phosphatase Shp2 (PTPN11) in cancer. Cancer Metastasis Rev 27 (2):179-192.
25. Kontaridis MI, Swanson KD, David FS, Barford D, Neel BG (2006) PTPN11 (Shp2) mutations in LEOPARD syndrome have dominant negative, not activating, effects. J Biol Chem 281 (10):6785-6792.
26. Ogata T, Yoshida R (2005) PTPN11 mutations and genotype-phenotype correlations in Noonan and LEOPARD syndromes. Pediatr Endocrinol Rev 2 (4):669-674.
27. Saxton TM, Pawson T (1999) Morphogenetic movements at gastrulation require the SH2 tyrosine phosphatase Shp2. Proc Natl Acad Sci USA 96 (7):3790-3795.
28. Saxton TM, et al. (1997) Abnormal mesoderm patterning in mouse embryos mutant for the SH2 tyrosine phosphatase Shp-2. EMBO J 16 (9):2352-2364.
29. Yu DH, Qu CK, Henegariu O, Lu X, Feng GS (1998) Protein-tyrosine phosphatase Shp-2 regulates cell spreading, migration, and focal adhesion. J Biol Chem 273 (33):21125-21131.
30. 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.
31. Connelly JT, et al. (2010) Actin and serum response factor transduce physical cues from the microenvironment to regulate epidermal stem cell fate decisions. Nat Cell Biol 12 (7):711-718.
32. Lee HH, Chang ZF (2008) Regulation of RhoA-dependent ROCKII activation by Shp2. J Cell Biol 181 (6):999-1012.
33. Lee HH, et al. (2010) Src-dependent phosphorylation of ROCK participates in regulation of focal adhesion dynamics. J Cell Sci 123 (Pt 19):3368-3377.
34. Prager-Khoutorsky M, et al. (2011) Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol 13 (12):1457-1465.
35. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA (2010) Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 6 (6):468-473.
36. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA (2010) Cell shape, spreading symmetry and the polarization of stress-fibers in cells. J Phys Condens Matter 22 (19): 194110.
37. Karlon WJ, et al. (1999) Measurement of orientation and distribution of cellular alignment and cytoskeletal organization. Ann Biomed Eng 27 (6):712-720.
38. Butler JP, Tolic-Nurrelykke IM, Fabry B, Fredberg JJ (2002) Traction fields, moments, and strain energy that cells exert on their surroundings. Am J Physiol Cell Physiol 282 (3):C595-C605.
39. Hur SS, et al. (2012) Roles of cell confluency and fluid shear in 3-dimensional intracellular forces in endothelial cells. Proc Natl Acad Sci USA 109 (28):11110-11115.
40. Kuo JC, Han X, Hsiao CT, Yates JR, 3rd, Waterman CM (2011) Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for p-Pix in negative regulation of focal adhesion maturation. Nat Cell Biol 13 (4):383-393.
41. Qu CK, et al. (1997) A deletion mutation in the SH2-N domain of Shp-2 severely suppresses hematopoietic cell development. Mol Cell Biol 17 (9):5499-5507.
42. Lo CM, Wang HB, Dembo M, Wang YL (2000) Cell movement is guided by the rigidity of the substrate. Biophys J 79 (1):144-152.
43. Vogel V, Sheetz M (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7 (4):265-275.
44. Giannone G, Sheetz MP (2006) Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol 16 (4):213-223.
45. Bao G, et al. (2010) Molecular biomechanics: The molecular basis of how forces regulate cellular function. Mol Cell Biomech 3 (2):91-105.
46. Mitra SK, Hanson DA, Schlaepfer DD (2005) Focal adhesion kinase: In command and control of cell motility. Nat Rev Mol Cell Biol 6 (1):56-68.
47. Burridge K, Sastry SK, Sallee JL (2006) Regulation of cell adhesion by protein-tyrosine phosphatases. I. Cell-matrix adhesion. J Biol Chem 281 (23):15593-15596.
48. Golji J, Wendorff T, Mofrad MR (2012) Phosphorylation primes vinculin for activation. Biophys J 102 (9):2022-2030.
49. Bregeon J, Loirand G, Pacaud P, Rolli-Derkinderen M (2009) Angiotensin II induces RhoA activation through SHP2-dependent dephosphorylation of the RhoGAP p190A in vascular smooth muscle cells. Am J Physiol Cell Physiol 297 (5):C1062-C1070.
50. Kontaridis MI, et al. (2004) SHP-2 positively regulates myogenesis by coupling to the Rho GTPase signaling pathway. Mol Cell Biol 24 (12):5340-5352.
51. Lacalle RA, et al. (2002) Specific SHP-2 partitioning in raft domains triggers integrin-mediated signaling via Rho activation. J Cell Biol 157 (2):277-289.
52. Schoenwaelder SM, et al. (2000) The protein tyrosine phosphatase Shp-2 regulates RhoA activity. Curr Biol 10 (23):1523-1526.
53. Kodama A, et al. (2000) Involvement of an SHP-2-Rho small G protein pathway in hepatocyte growth factor/scatter factor-induced cell scattering. Mol Biol Cell 11 (8):2565-2575.
54. Zhang SQ, et al. (2004) Shp2 regulates SRC family kinase activity and Ras/Erk activation by controlling Csk recruitment. Mol Cell 13 (3):341-355.
55. Chuang HH, et al. (2012) ROCKII Ser1366 phosphorylation reflects the activation status. Biochem J 443 (1):145-151.
56. von Wichert G, Haimovich B, Feng GS, Sheetz MP (2003) Force-dependent integrin-cytoskeleton linkage formation requires downregulation of focal complex dynamics by Shp2. EMBO J 22 (19):5023-5035.
57. Wang YL, Pelham RJ, Jr. (1998) Preparation of a flexible, porous polyacrylamide substrate for mechanical studies of cultured cells. Methods Enzymol 298:489-496.
58. Hur SS, Zhao Y, Li YS, Botvinick E, Chien S (2009) Live cells exert 3-dimensional traction forces on their substrata. Cell Mol Bioeng 2 (3):425-436.