Unfolding dynamics of the mucin SEA domain probed by force spectroscopy suggest that it acts as a cell-protective device

FEBS Journal

Volumn 280, Issue 6, 2013, Pages 1491-1501

  Pelaseyed, Thaher ^a   Zäch, Michael ^b   Petersson, Åsa C ^a   Svensson, Frida ^a   Johansson, Denny G A ^a   Hansson, Gunnar C ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

atomic force microscopy; MUC1; mucin; SEA domain; single molecule force spectroscopy

Indexed keywords

RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; ATOMIC FORCE MICROSCOPY; CELL MEMBRANE; CELL PROTECTION; CELL SURFACE; CONTROLLED STUDY; FORCE; MECHANICAL FORCE; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTECTIVE EQUIPMENT; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN UNFOLDING; SEA DOMAIN; TEMPERATURE SENSITIVITY;

ANIMALS; BIOMECHANICS; CELL MEMBRANE; CHO CELLS; CRICETINAE; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICROSCOPY, ATOMIC FORCE; MODELS, MOLECULAR; MUCIN-1; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN STABILITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN UNFOLDING; PROTEOLYSIS; RECOMBINANT PROTEINS; STRESS, MECHANICAL; TEMPERATURE; TRANSFECTION;

ECHINOIDEA;

EID: 84875372900     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12144     Document Type: Article

References (43)

1. McGuckin MA, Lindén SK, Sutton P, &, Florin TH, (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9, 265-278.
2. Gendler SJ, &, Spicer AP, (1995) Epithelial mucin genes. Annu Rev Physiol 57, 607-634.
3. Hattrup CL, &, Gendler SJ, (2008) Structure and function of the cell surface (tethered) mucins. Annu Rev Physiol 70, 431-457.
4. Lillehoj EP, Kim H, Chun EY, &, Kim KC, (2004) Pseudomonas aeruginosa stimulates phosphorylation of the airway epithelial membrane glycoprotein Muc1 and activates MAP kinase. Am J Physiol Lung Cell Mol Physiol 287, L809-815.
5. Gendler SJ, (2001) MUC1, the renaissance molecule. J Mammary Gland Biol Neoplasia 6, 339-353.
6. Lillehoj ER, &, Kim KC, (2002) Airway mucus: its components and function. Arch Pharm Res 25, 770-780.
7. Hartman M, Baruch A, Ron I, Aderet Y, Yoeli M, Sagi-Assif O, Greenstein S, Stadler Y, Weiss M, Harness E, et al,. (1999) MUC1 isoform specific monoclonal antibody 6E6/2 detects preferential expression of the novel MUC1/Y protein in breast and ovarian cancer. Int J Cancer 82, 256-267.
8. Hinojosa-Kurtzberg AM, Johansson ME, Madsen CS, Hansson GC, &, Gendler SJ, (2003) Novel MUC1 splice variants contribute to mucin overexpression in CFTR-deficient mice. Am J Physiol 284, G853-862.
9. Baruch A, Hartmann M, Yoeli M, Adereth Y, Greenstein S, Stadler Y, Skornik Y, Zaretsky J, Smorodinsky NI, Keydar I, et al,. (1999) The breast cancer-associated MUC1 gene generates both a receptor and its cognate binding protein. Cancer Res 59, 1552-1561.
10. Bork P, &, Patthy L, (1995) The SEA module: a new extracellular domain associated with O-glycosylation. Protein Sci 4, 1421-1425.
11. Ligtenberg MJ, Kruijshaar L, Buijs F, van Meijer M, Litvinov SV, &, Hilkens J, (1992) Cell-associated episialin is a complex containing two proteins derived from a common precursor. J Biol Chem 267, 6171-6177.
12. Macao B, Johansson DG, Hansson GC, &, Hard T, (2006) Autoproteolysis coupled to protein folding in the SEA domain of the membrane-bound MUC1 mucin. Nat Struct Mol Biol 13, 71-76.
13. Parry S, Silverman HS, McDermott K, Willis A, Hollingsworth MA, &, Harris A, (2001) Identification of MUC1 proteolytic cleavage sites in vivo. Biochem Biophys Res Commun 283, 715-720.
14. Levitin F, Stern O, Weiss M, Gil-Henn C, Ziv R, Prokocimer Z, Smorodinsky NI, Rubinstein DB, &, Wreschner DH, (2005) The MUC1 SEA module is a self-cleaving domain. J Biol Chem 280, 33374-33386.
15. Johansson DG, Wallin G, Sandberg A, Macao B, Aqvist J, &, Hard T, (2009) Protein autoproteolysis: conformational strain linked to the rate of peptide cleavage by the pH dependence of the N ↠O acyl shift reaction. J Am Chem Soc 131, 9475-9477.
16. Johansson DGA, Macao B, Sandberg A, &, Härd T, (2008) SEA domain autoproteolysis accelerated by conformational strain: mechanistic aspects. J Mol Biol 377, 1130-1143.
17. Marko JF, &, Siggia ED, (1995) Stretching DNA. Macromolecules 28, 8759-8770.
18. Bustamante C, Marko JF, Siggia ED, &, Smith S, (1994) Entropic elasticity of lambda-phage DNA. Science 265, 1599-1600.
19. Kratky O, &, Porod G, (1949) Diffuse small-angle scattering of X-rays in colloid systems. J Colloid Sci 4, 35-70.
20. Grutzner A, Garcia-Manyes S, Kotter S, Badilla CL, Fernandez JM, &, Linke WA, (2009) Modulation of titin-based stiffness by disulfide bonding in the cardiac titin N2-B unique sequence. Biophys J 97, 825-834.
21. Janshoff A, Neitzert M, Oberdorfer Y, &, Fuchs H, (2000) Force spectroscopy of molecular systems-single molecule spectroscopy of polymers and biomolecules. Angew Chem Int Ed Engl 39, 3212-3237.
22. Verbelen C, Gruber HJ, &, Dufrene YF, (2007) The NTA-His6 bond is strong enough for AFM single-molecular recognition studies. J Mol Recognit 20, 490-494.
23. Grandbois M, Beyer M, Rief M, Clausen-Schaumann H, &, Gaub HE, (1999) How strong is a covalent bond? Science 283, 1727-1730.
24. Andrea A, &, Paolo F, (2005) AFM: a versatile tool in biophysics. Meas Sci Technol 16, R65.
25. Marszalek PE, Lu H, Li H, Carrion-Vazquez M, Oberhauser AF, Schulten K, &, Fernandez JM, (1999) Mechanical unfolding intermediates in titin modules. Nature 402, 100-103.
26. Peng Q, &, Li H, (2008) Atomic force microscopy reveals parallel mechanical unfolding pathways of T4 lysozyme: evidence for a kinetic partitioning mechanism. Proc Natl Acad Sci USA 105, 1885-1890.
27. Akhavan A, Crivelli SN, Singh M, Lingappa VR, &, Muschler JL, (2008) SEA domain proteolysis determines the functional composition of dystroglycan. FASEB J 22, 612-621.
28. Singh PK, &, Hollingsworth MA, (2006) Cell surface-associated mucins in signal transduction. Trends Cell Biol 16, 467-476.
29. Pitoniak A, Birkaya B, Dionne HM, Vadaie N, &, Cullen PJ, (2009) The signaling mucins Msb2 and Hkr1 differentially regulate the filamentation mitogen-activated protein kinase pathway and contribute to a multimodal response. Mol Biol Cell 20, 3101-3114.
30. Tatebayashi K, Tanaka K, Yang HY, Yamamoto K, Matsushita Y, Tomida T, Imai M, &, Saito H, (2007) Transmembrane mucins Hkr1 and Msb2 are putative osmosensors in the SHO1 branch of yeast HOG pathway. EMBO J 26, 3521-3533.
31. Kesimer M, &, Sheehan JK, (2008) Analyzing the functions of large glycoconjugates through the dissipative properties of their absorbed layers using the gel-forming mucin MUC5B as an example. Glycobiology 18, 463-472.
32. Kufe DW, (2009) Mucins in cancer: function, prognosis and therapy. Nat Rev Cancer 9, 874-885.
33. Malmberg EK, Pelaseyed T, Petersson AC, Seidler UE, De Jonge H, Riordan JR, &, Hansson GC, (2008) The C-terminus of the transmembrane mucin MUC17 binds to the scaffold protein PDZK1 that stably localizes it to the enterocyte apical membrane in the small intestine. Biochem J 410, 283-289.
34. Pelaseyed T, &, Hansson GC, (2011) CFTR anion channel modulates expression of human transmembrane mucin MUC3 through the PDZ protein GOPC. J Cell Sci 124, 3074-3083.
35. Florin EL, Moy VT, &, Gaub HE, (1994) Adhesion forces between individual ligand-receptor pairs. Science 264, 415-417.
36. Bertz M, Wilmanns M, &, Rief M, (2009) The titin-telethonin complex is a directed, superstable molecular bond in the muscle Z-disk. Proc Natl Acad Sci USA 106, 13307-13310.
37. Button B, Cai LH, Ehre C, Kesimer M, Hill DB, Sheehan JK, Boucher RC, &, Rubinstein M, (2012) A periciliary brush promotes the lung health by separating the mucus layer from airway epithelia. Science 337, 937-941.
38. Hill DB, Swaminathan V, Estes A, Cribb J, O'Brien ET, Davis CW, &, Superfine R, (2010) Force generation and dynamics of individual cilia under external loading. Biophys J 98, 57-66.
39. Afrin R, Arakawa H, Osada T, &, Ikai A, (2003) Extraction of membrane proteins from a living cell surface using the atomic force microscope and covalent crosslinkers. Cell Biochem Biophys 39, 101-117.
40. Kubitschek HE, (1990) Cell volume increase in Escherichia coli after shifts to richer media. J Bacteriol 172, 94-101.
41. Lidell ME, Johansson ME, Morgelin M, Asker N, Gum JR Jr, Kim YS, &, Hansson GC, (2003) The recombinant C-terminus of the human MUC2 mucin forms dimers in Chinese hamster ovary cells and heterodimers with full-length MUC2 in LS 174T cells. Biochem J 372, 335-345.
42. Swain M, &, Ross NW, (1995) A silver stain protocol for proteins yielding high resolution and transparent background in sodium dodecyl sulfate-polyacrylamide gels. Electrophoresis 16, 948-951.
43. Jeffrey LH, &, John B, (1993) Calibration of atomic-force microscope tips. Rev Sci Instrum 64, 1868-1873.