Serum inter-α-inhibitor activates the yes tyrosine kinase and YAP/TEAD transcriptional complex in mouse embryonic stem cells

Journal of Biological Chemistry

Volumn 289, Issue 48, 2014, Pages 33492-33502

  Pijuan Galitó, Sara ^a   Tamm, Christoffer ^a   Annerén, Cecilia ^a,b  

^a UPPSALA UNIVERSITY   (Sweden)

^b GE Healthcare Bio Sciences AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL CULTURE; CHEMICAL ACTIVATION; ENZYMES; MAMMALS; STEM CELLS; TRANSCRIPTION;

AUTOPHOSPHORYLATION; BOVINE SERUM ALBUMINS; CELL CULTURE MEDIUMS; DOSE-DEPENDENT MANNER; LEUKEMIA INHIBITORY FACTORS; MOUSE EMBRYONIC STEM CELLS; NUCLEAR LOCALIZATION; TRANSCRIPTIONAL COMPLEXES;

BODY FLUIDS;

BOVINE SERUM ALBUMIN; INTER ALPHA INHIBITOR; OCTAMER TRANSCRIPTION FACTOR 4; ORGANIC CATION TRANSPORTER 3; PLASMA PROTEIN; PROTEIN KINASE YES; PROTEIN TEAD; PROTEIN YAP; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG; ALPHA GLOBULIN; DNA BINDING PROTEIN; INTER-ALPHA-INHIBITOR; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TEAD2 PROTEIN, HUMAN; TEAD2 PROTEIN, MOUSE; YAP PROTEIN, MOUSE; YAP1 (YES-ASSOCIATED) PROTEIN, HUMAN; YES1 PROTEIN, HUMAN; YES1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; AUTOPHOSPHORYLATION; CULTURE MEDIUM; EMBRYONIC STEM CELL; ENZYME ACTIVATION; GENETIC TRANSCRIPTION; HEAVY CHAIN; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SERUM; TRANSCRIPTION INITIATION; ANIMAL; BOVINE; CELL NUCLEUS; CYTOLOGY; GENETICS; METABOLISM; PHYSIOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALPHA-GLOBULINS; ANIMALS; CATTLE; CELL NUCLEUS; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; ENZYME ACTIVATION; HUMANS; MICE; PHOSPHOPROTEINS; PLURIPOTENT STEM CELLS; PROTO-ONCOGENE PROTEINS C-YES; TRANSCRIPTION FACTORS;

EID: 84912120143     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.580076     Document Type: Article

References (51)

1. Chambers, I., and Smith, A. (2004) Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23, 7150-7160
2. Xiao, L., Yuan, X., and Sharkis, S. J. (2006) Activin A maintains self-renewal and regulates fibroblast growth factor, Wnt, and bone morphogenic protein pathways in human embryonic stem cells. Stem Cells 24, 1476-1486
3. Vallier, L., Alexander, M., and Pedersen, R. A. (2005) Activin/Nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J. Cell Sci. 118, 4495-4509
4. Miyazaki, T., Futaki, S., Suemori, H., Taniguchi, Y., Yamada, M., Kawasaki, M., Hayashi, M., Kumagai, H., Nakatsuji, N., Sekiguchi, K., and Kawase, E. (2012) Laminin E8 fragments support efficient adhesion and expansion of dissociated human pluripotent stem cells. Nature Commun. 3, 1236
5. Braam, S. R., Zeinstra, L., Litjens, S., Ward-van Oostwaard, D., van den Brink, S., van Laake, L., Lebrin, F., Kats, P., Hochstenbach, R., Passier, R., Sonnenberg, A., and Mummery, C. L. (2008) Recombinant vitronectin is a functionally defined substrate that supports human embryonic stem cell self-renewal via αvβ5 integrin. Stem Cells 26, 2257-2265
6. Melkoumian, Z., Weber, J. L., Weber, D. M., Fadeev, A. G., Zhou, Y., Dolley-Sonneville, P., Yang, J., Qiu, L., Priest, C. A., Shogbon, C., Martin, A. W., Nelson, J., West, P., Beltzer, J. P., Pal, S., and Brandenberger, R. (2010) Synthetic peptide-acrylate surfaces for long-term self-renewal and cardiomyocyte differentiation of human embryonic stem cells. Nature Biotechnology 28, 606-610
7. Ilic, D. (2006) Culture of human embryonic stem cells and the extracellular matrix microenvironment. Regenerative Med. 1, 95-101
8. Stojkovic, P., Lako, M., Przyborski, S., Stewart, R., Armstrong, L., Evans, J., Zhang, X., and Stojkovic, M. (2005) Human-serum matrix supports undifferentiated growth of human embryonic stem cells. Stem Cells 23, 895-902
9. Annerén, C. (2008) Tyrosine kinase signalling in embryonic stem cells. Clin. Sci. 115, 43-55
10. Betschinger, J., Nichols, J., Dietmann, S., Corrin, P. D., Paddison, P. J., and Smith, A. (2013) Exit from pluripotency is gated by intracellular redistribution of the bHLH transcription factor Tfe3. Cell 153, 335-347
11. Tamm, C., Bower, N., and Annerén, C. (2011) Regulation of mouse embryonic stem cell self-renewal by a Yes-YAP-TEAD2 signaling pathway downstream of LIF. J. Cell Sci. 124, 1136-1144
12. Lian, I., Kim, J., Okazawa, H., Zhao, J., Zhao, B., Yu, J., Chinnaiyan, A., Israel, M. A., Goldstein, L. S., Abujarour, R., Ding, S., and Guan, K. L. (2010) The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev. 24, 1106-1118
13. Annerén, C., Cowan, C. A., and Melton, D. A. (2004) The Src family of tyrosine kinases is important for embryonic stem cell self-renewal. J. Biol. Chem. 279, 31590-31598
14. Vassilev, A., Kaneko, K. J., Shu, H., Zhao, Y., and DePamphilis, M. L. (2001) TEAD/TEF transcription factors utilize the activation domain of YAP65, a Src/Yes-associated protein localized in the cytoplasm. Genes Dev. 15, 1229-1241
15. Zhang, X., Meyn, M. A., 3rd, and Smithgall, T. E. (2014) c-Yes tyrosine kinase is a potent suppressor of ES cell differentiation and antagonizes the actions of its closest phylogenetic relative, c-Src. ACS chemical biology 9, 139-146
16. Josic, D., Brown, M. K., Huang, F., Lim, Y. P., Rucevic, M., Clifton, J. G., and Hixson, D. C. (2006) Proteomic characterization of inter-α inhibitor proteins from human plasma. Proteomics 6, 2874-2885
17. Jessen, T. E., and Ødum, L. (2003) Role of tumour necrosis factor stimulated gene 6 (TSG-6) in the coupling of inter-α-trypsin inhibitor to hyaluronan in human follicular fluid. Reproduction 125, 27-31
18. Smith, A. (1991) Culture and differentiation of embryonic stem cells. Methods in Cell Science 13, 89-94
19. Ying, Q. L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., and Smith, A. (2008) The ground state of embryonic stem cell self-renewal. Nature 453, 519-523
20. Li, P., Tong, C., Mehrian-Shai, R., Jia, L., Wu, N., Yan, Y., Maxson, R. E., Schulze, E. N., Song, H., Hsieh, C. L., Pera, M. F., and Ying, Q. L. (2008) Germline competent embryonic stem cells derived from rat blastocysts. Cell 135, 1299-1310
21. Ludwig, T. E., Bergendahl, V., Levenstein, M. E., Yu, J., Probasco, M. D., and Thomson, J. A. (2006) Feeder-independent culture of human embryonic stem cells. Nature Methods 3, 637-646
22. Lei, T., He, Q. Y., Wang, Y. L., Si, L. S., and Chiu, J. F. (2008) Heparin chromatography to deplete high-abundance proteins for serum proteomics. Clin. Chim. Acta 388, 173-178
23. Arakawa, T., Tsumoto, K., Ejima, D., Kita, Y., Yonezawa, Y., and Tokunaga, M. (2007) Induced binding of proteins by ammonium sulfate in affinity and ion-exchange column chromatography. J. Biochem. Biophys. Methods 70, 493-498
24. Blom, A. M., Mörgelin, M., Oyen, M., Jarvet, J., and Fries, E. (1999) Structural characterization of inter-α-inhibitor. Evidence for an extended shape. J. Biol. Chem. 274, 298-304
25. Enghild, J. J., Thøgersen, I. B., Pizzo, S. V., and Salvesen, G. (1989) Analysis of inter-α-trypsin inhibitor and a novel trypsin inhibitor, pre-α-trypsin inhibitor, from human plasma. Polypeptide chain stoichiometry and assembly by glycan. J. Biol. Chem. 264, 15975-15981
26. Jiang, S. W., and Eberhardt, N. L. (1995) Involvement of a protein distinct from transcription enhancer factor-1 (TEF-1) in mediating human chorionic somatomammotropin gene enhancer function through the GT-IIC enhanson in choriocarcinoma and COS cells. J. Biol. Chem. 270, 13906-13915
27. Hattori, N., Imao, Y., Nishino, K., Hattori, N., Ohgane, J., Yagi, S., Tanaka, S., and Shiota, K. (2007) Epigenetic regulation of Nanog gene in embryonic stem and trophoblast stem cells. Genes Cells 12, 387-396
28. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
29. Ying, Q. L., Nichols, J., Chambers, I., and Smith, A. (2003) BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115, 281-292
30. Varelas, X., Sakuma, R., Samavarchi-Tehrani, P., Peerani, R., Rao, B. M., Dembowy, J., Yaffe, M. B., Zandstra, P. W., and Wrana, J. L. (2008) TAZ controls Smad nucleocytoplasmic shuttling and regulates human embryonic stem-cell self-renewal. Nature Cell Biology 10, 837-848
31. Hess, K. A., Chen, L., and Larsen, W. J. (1999) Inter-α-inhibitor binding to hyaluronan in the cumulus extracellular matrix is required for optimal ovulation and development of mouse oocytes. Biol. Reprod. 61, 436-443
32. He, H., Li, W., Tseng, D. Y., Zhang, S., Chen, S. Y., Day, A. J., and Tseng, S. C. (2009) Biochemical characterization and function of complexes formed by hyaluronan and the heavy chains of inter-α-inhibitor (HC∗HA) purified from extracts of human amniotic membrane. J. Biol. Chem. 284, 20136-20146
33. Werbowetski-Ogilvie, T. E., Agar, N. Y., Waldkircher de Oliveira, R. M., Faury, D., Antel, J. P., Jabado, N., and Del Maestro, R. F. (2006) Isolation of a natural inhibitor of human malignant glial cell invasion: inter α-trypsin inhibitor heavy chain 2. Cancer Res. 66, 1464-1472
34. Adair, J. E., Stober, V., Sobhany, M., Zhuo, L., Roberts, J. D., Negishi, M., Kimata, K., and Garantziotis, S. (2009) Inter-α-trypsin inhibitor promotes bronchial epithelial repair after injury through vitronectin binding. J. Biol. Chem. 284, 16922-16930
35. Zhao, B., Ye, X., Yu, J., Li, L., Li, W., Li, S., Yu, J., Lin, J. D., Wang, C. Y., Chinnaiyan, A. M., Lai, Z. C., and Guan, K. L. (2008) TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962-1971
36. Lai, D., Ho, K. C., Hao, Y., and Yang, X. (2011) Taxol resistance in breast cancer cells is mediated by the hippo pathway component TAZ and its downstream transcriptional targets Cyr61 and CTGF. Cancer Res. 71, 2728-2738
37. Zhang, H., Liu, C. Y., Zha, Z. Y., Zhao, B., Yao, J., Zhao, S., Xiong, Y., Lei, Q. Y., and Guan, K. L. (2009) TEAD transcription factors mediate the function of TAZ in cell growth and epithelial-mesenchymal transition. J. Biol. Chem. 284, 13355-13362
38. Tamm, C., Pijuan Galitó, S., and Anneren, C. (2013) A comparative study of protocols for mouse embryonic stem cell culturing. PloS one 8, e81156
39. Zhao, B., Li, L., Lei, Q., and Guan, K. L. (2010) The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev. 24, 862-874
40. Levy, D., Adamovich, Y., Reuven, N., and Shaul, Y. (2008) Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol. Cell 29, 350-361
41. Zhao, M., Yoneda, M., Ohashi, Y., Kurono, S., Iwata, H., Ohnuki, Y., and Kimata, K. (1995) Evidence for the covalent binding of SHAP, heavy chains of inter-α-trypsin inhibitor, to hyaluronan. J. Biol. Chem. 270, 26657-26663
42. Garantziotis, S., Zudaire, E., Trempus, C. S., Hollingsworth, J. W., Jiang, D., Lancaster, L. H., Richardson, E., Zhuo, L., Cuttitta, F., Brown, K. K., Noble, P. W., Kimata, K., and Schwartz, D. A. (2008) Serum inter-α-trypsin inhibitor and matrix hyaluronan promote angiogenesis in fibrotic lung injury. Am. J. Respir. Crit. Care Med. 178, 939-947
43. Garantziotis, S., Hollingsworth, J. W., Ghanayem, R. B., Timberlake, S., Zhuo, L., Kimata, K., and Schwartz, D. A. (2007) Inter-α-trypsin inhibitor attenuates complement activation and complement-induced lung injury. J. Immunol. 179, 4187-4192
44. Zhang, S., He, H., Day, A. J., and Tseng, S. C. (2012) Constitutive expression of inter-α-inhibitor (IαI) family proteins and tumor necrosis factor-stimulated gene-6 (TSG-6) by human amniotic membrane epithelial and stromal cells supporting formation of the heavy chain-hyaluronan (HC-HA) complex. J. Biol. Chem. 287, 12433-12444
45. Sanggaard, K. W., Sonne-Schmidt, C. S., Krogager, T. P., Lorentzen, K. A., Wisniewski, H. G., Thøgersen, I. B., and Enghild, J. J. (2008) The transfer of heavy chains from bikunin proteins to hyaluronan requires both TSG-6 and HC2. J. Biol. Chem. 283, 18530-18537
46. Shay, E., He, H., Sakurai, S., and Tseng, S. C. (2011) Inhibition of angiogenesis by HC.HA, a complex of hyaluronan and the heavy chain of inter-α-inhibitor, purified from human amniotic membrane. Invest. Ophthalmol. Vis. Sci. 52, 2669-2678
47. Tan, K. T., Baildam, A. D., Juma, A., Milner, C. M., Day, A. J., and Bayat, A. (2011) Hyaluronan, TSG-6, and inter-α-inhibitor in periprosthetic breast capsules: reduced levels of free hyaluronan and TSG-6 expression in contracted capsules. Aesthet. Surg. J. 31, 47-55
48. Shimabukuro, Y., Terashima, H., Takedachi, M., Maeda, K., Nakamura, T., Sawada, K., Kobashi, M., Awata, T., Oohara, H., Kawahara, T., Iwayama, T., Hashikawa, T., Yanagita, M., Yamada, S., and Murakami, S. (2011) Fibroblast growth factor-2 stimulates directed migration of periodontal ligament cells via PI3K/AKT signaling and CD44/hyaluronan interaction. J. Cell. Physiol. 226, 809-821
49. Jin, Y. J., Park, I., Hong, I. K., Byun, H. J., Choi, J., Kim, Y. M., and Lee, H. (2011) Fibronectin and vitronectin induce AP-1-mediated matrix metal-loproteinase- 9 expression through integrin α(5)β(1)/α(v)β(3)-dependent Akt, ERK and JNK signaling pathways in human umbilical vein endothelial cells. Cell. Signal. 23, 125-134
50. Musah, S., Morin, S. A., Wrighton, P. J., Zwick, D. B., Jin, S., and Kiessling, L. L. (2012) Glycosaminoglycan-binding hydrogels enable mechanical control of human pluripotent stem cell self-renewal. ACS nano 6, 10168-10177
51. Dupont, S., Morsut, L., Aragona, M., Enzo, E., Giulitti, S., Cordenonsi, M., Zanconato, F., Le Digabel, J., Forcato, M., Bicciato, S., Elvassore, N., and Piccolo, S. (2011) Role of YAP/TAZ in mechanotransduction. Nature 474, 179-183