Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Annexins Bend Wound Edges during Plasma Membrane Repair

Author(s): Adam Cohen Simonsen*, Theresa Louise Boye and Jesper Nylandsted*

Volume 27, Issue 22, 2020

Page: [3600 - 3610] Pages: 11

DOI: 10.2174/0929867326666190121121143

Price: $65

Abstract

The plasma membrane of eukaryotic cells defines the boundary to the extracellular environment and, thus provides essential protection from the surroundings. Consequently, disruptions to the cell membrane triggered by excessive mechanical or biochemical stresses pose fatal threats to cells, which they need to cope with to survive. Eukaryotic cells cope with these threats by activating their plasma membrane repair system, which is shared by other cellular functions, and includes mechanisms to remove damaged membrane by internalization (endocytosis), shedding, reorganization of cytoskeleton and membrane fusion events to reseal the membrane. Members of the annexin protein family, which are characterized by their Ca2+-dependent binding to anionic phospholipids, are important regulators of plasma membrane repair. Recent studies based on cellular and biophysical membrane models show that they have more distinct functions in the repair response than previously assumed by regulating membrane curvature and excision of damaged membrane. In cells, plasma membrane injury and flux of Ca2+ ions into the cytoplasm trigger recruitment of annexins including annexin A4 and A6 to the membrane wound edges. Here, they induce curvature and constriction force, which help pull the wound edges together for eventual fusion. Cancer cells are dependent on efficient plasma membrane repair to counteract frequent stress-induced membrane injuries, which opens novel avenues to target cancer cells through their membrane repair system. Here, we discuss mechanisms of single cell wound healing implicating annexin proteins and membrane curvature.

Keywords: Annexin, plasma membrane repair, membrane curvature, membrane injury, cancer, annexin A4, annexin A6.

[1]
Grewal, T.; Wason, S.J.; Enrich, C.; Rentero, C. Annexins - insights from knockout mice. Biol. Chem., 2016, 397(10), 1031-1053.
[http://dx.doi.org/10.1515/hsz-2016-0168] [PMID: 27318360]
[2]
Boye, T.L.; Nylandsted, J. Annexins in plasma membrane repair. Biol. Chem., 2016, 397(10), 961-969.
[http://dx.doi.org/10.1515/hsz-2016-0171] [PMID: 27341560]
[3]
Moss, S.E.; Morgan, R.O. The annexins. Genome Biol., 2004, 5(4), 219.
[http://dx.doi.org/10.1186/gb-2004-5-4-219] [PMID: 15059252]
[4]
Clark, G.B.; Morgan, R.O.; Fernandez, M.P.; Roux, S.J. Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytol., 2012, 196(3), 695-712.
[http://dx.doi.org/10.1111/j.1469-8137.2012.04308.x] [PMID: 22994944]
[5]
Morgan, R.O.; Martin-Almedina, S.; Iglesias, J.M.; Gonzalez-Florez, M.I.; Fernandez, M.P. Evolutionary perspective on annexin calcium-binding domains. Biochim. Biophys. Acta, 2004, 1742(1-3), 133-140.
[http://dx.doi.org/10.1016/j.bbamcr.2004.09.010] [PMID: 15590063]
[6]
Morgan, R.O.; Pilar Fernandez, M. Distinct annexin subfamilies in plants and protists diverged prior to animal annexins and from a common ancestor. J. Mol. Evol., 1997, 44(2), 178-188.
[http://dx.doi.org/10.1007/PL00006134] [PMID: 9069178]
[7]
Swairjo, M.A.; Concha, N.O.; Kaetzel, M.A.; Dedman, J.R.; Seaton, B.A. Ca(2+)-bridging mechanism and phospholipid head group recognition in the membrane-binding protein annexin V. Nat. Struct. Biol., 1995, 2(11), 968-974.
[http://dx.doi.org/10.1038/nsb1195-968] [PMID: 7583670]
[8]
Gerke, V.; Creutz, C.E.; Moss, S.E. Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol., 2005, 6(6), 449-461.
[http://dx.doi.org/10.1038/nrm1661] [PMID: 15928709]
[9]
Meers, P.; Mealy, T. Calcium-dependent annexin V binding to phospholipids: stoichiometry, specificity, and the role of negative charge. Biochemistry, 1993, 32(43), 11711-11721.
[http://dx.doi.org/10.1021/bi00094a030] [PMID: 8218240]
[10]
Geisow, M.J.; Walker, J.H.; Boustead, C.; Taylor, W. Localization and structure of novel calcium-regulated phospholipid-binding proteins. Biochem. Soc. Trans., 1987, 15(5), 800-802.
[http://dx.doi.org/10.1042/bst0150800] [PMID: 3319735]
[11]
Lizarbe, M.A.; Barrasa, J.I.; Olmo, N.; Gavilanes, F.; Turnay, J. Annexin-phospholipid interactions. Functional implications. Int. J. Mol. Sci., 2013, 14(2), 2652-2683.
[http://dx.doi.org/10.3390/ijms14022652] [PMID: 23358253]
[12]
Geisow, M.J.; Walker, J.H.; Boustead, C.; Taylor, W. Annexins--new family of Ca2+-regulated-phospholipid binding protein. Biosci. Rep., 1987, 7(4), 289-298.
[http://dx.doi.org/10.1007/BF01121450] [PMID: 2960386]
[13]
Cooper, S.T.; McNeil, P.L. Membrane repair: mechanisms and pathophysiology. Physiol. Rev., 2015, 95(4), 1205-1240.
[http://dx.doi.org/10.1152/physrev.00037.2014] [PMID: 26336031]
[14]
Demonbreun, A.R.; Quattrocelli, M.; Barefield, D.Y.; Allen, M.V.; Swanson, K.E.; McNally, E.M. An actin-dependent annexin complex mediates plasma membrane repair in muscle. J. Cell Biol., 2016, 213(6), 705-718.
[http://dx.doi.org/10.1083/jcb.201512022] [PMID: 27298325]
[15]
Gerke, V.; Moss, S.E. Annexins: from structure to function. Physiol. Rev., 2002, 82(2), 331-371.
[http://dx.doi.org/10.1152/physrev.00030.2001] [PMID: 11917092]
[16]
Barton, G.J.; Newman, R.H.; Freemont, P.S.; Crumpton, M.J. Amino acid sequence analysis of the annexin super-gene family of proteins. Eur. J. Biochem., 1991, 198(3), 749-760.
[http://dx.doi.org/10.1111/j.1432-1033.1991.tb16076.x] [PMID: 1646719]
[17]
Lauritzen, S.P.; Boye, T.L.; Nylandsted, J. Annexins are instrumental for efficient plasma membrane repair in cancer cells. Semin. Cell Dev. Biol., 2015, 45, 32-38.
[http://dx.doi.org/10.1016/j.semcdb.2015.10.028] [PMID: 26498035]
[18]
Turnay, J.; Lecona, E.; Fernández-Lizarbe, S.; Guzmán-Aránguez, A.; Fernández, M.P.; Olmo, N.; Lizarbe, M.A. Structure-function relationship in annexin A13, the founder member of the vertebrate family of annexins. Biochem. J., 2005, 389(Pt 3), 899-911.
[http://dx.doi.org/10.1042/BJ20041918] [PMID: 15813707]
[19]
Brownawell, A.M.; Creutz, C.E. Calcium-dependent binding of sorcin to the N-terminal domain of synexin (annexin VII). J. Biol. Chem., 1997, 272(35), 22182-22190.
[http://dx.doi.org/10.1074/jbc.272.35.22182] [PMID: 9268363]
[20]
Smith, P.D.; Davies, A.; Crumpton, M.J.; Moss, S.E. Structure of the human annexin VI gene. Proc. Natl. Acad. Sci. USA, 1994, 91(7), 2713-2717.
[http://dx.doi.org/10.1073/pnas.91.7.2713] [PMID: 8146179]
[21]
Rintala-Dempsey, A.C.; Rezvanpour, A.; Shaw, G.S. S100-annexin complexes--structural insights. FEBS J., 2008, 275(20), 4956-4966.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06654.x] [PMID: 18795951]
[22]
Dempsey, A.C.; Walsh, M.P.; Shaw, G.S. Unmasking the annexin I interaction from the structure of Apo-S100A11. Structure, 2003, 11(7), 887-897.
[http://dx.doi.org/10.1016/S0969-2126(03)00126-6] [PMID: 12842051]
[23]
Lewit-Bentley, A.; Réty, S.; Sopkova-de Oliveira Santos, J.; Gerke, V. S100-annexin complexes: some insights from structural studies. Cell Biol. Int., 2000, 24(11), 799-802.
[http://dx.doi.org/10.1006/cbir.2000.0629] [PMID: 11067764]
[24]
Rezvanpour, A.; Santamaria-Kisiel, L.; Shaw, G.S. The S100A10-annexin A2 complex provides a novel asymmetric platform for membrane repair. J. Biol. Chem., 2011, 286(46), 40174-40183.
[http://dx.doi.org/10.1074/jbc.M111.244038] [PMID: 21949189]
[25]
Miwa, N.; Uebi, T.; Kawamura, S. S100-annexin complexes--biology of conditional association. FEBS J., 2008, 275(20), 4945-4955.
[http://dx.doi.org/10.1111/j.1742-4658.2008.06653.x] [PMID: 18795952]
[26]
Rintala-Dempsey, A.C.; Santamaria-Kisiel, L.; Liao, Y.; Lajoie, G.; Shaw, G.S. Insights into S100 target specificity examined by a new interaction between S100A11 and annexin A2. Biochemistry, 2006, 45(49), 14695-14705.
[http://dx.doi.org/10.1021/bi061754e] [PMID: 17144662]
[27]
Santamaria-Kisiel, L.; Rintala-Dempsey, A.C.; Shaw, G.S. Calcium-dependent and -independent interactions of the S100 protein family. Biochem. J., 2006, 396(2), 201-214.
[http://dx.doi.org/10.1042/BJ20060195] [PMID: 16683912]
[28]
Sonnemann, K.J.; Bement, W.M. Wound repair: toward understanding and integration of single-cell and multicellular wound responses. Annu. Rev. Cell Dev. Biol., 2011, 27, 237-263.
[http://dx.doi.org/10.1146/annurev-cellbio-092910-154251] [PMID: 21721944]
[29]
Abreu-Blanco, M.T.; Verboon, J.M.; Parkhurst, S.M. Single cell wound repair: Dealing with life’s little traumas. Bioarchitecture, 2011, 1(3), 114-121.
[http://dx.doi.org/10.4161/bioa.1.3.17091] [PMID: 21922041]
[30]
Horn, A.; Jaiswal, J.K. Cellular mechanisms and signals that coordinate plasma membrane repair. Cell. Mol. Life Sci., 2018, 75(20), 3751-3770.
[http://dx.doi.org/10.1007/s00018-018-2888-7] [PMID: 30051163]
[31]
Cooper, S.T.; Head, S.I. Membrane injury and repair in the muscular dystrophies. Neuroscientist, 2015, 21(6), 653-668.
[http://dx.doi.org/10.1177/1073858414558336] [PMID: 25406223]
[32]
Cong, X.; Hubmayr, R.D.; Li, C.; Zhao, X. Plasma membrane wounding and repair in pulmonary diseases. Am. J. Physiol. Lung Cell. Mol. Physiol., 2017, 312(3), L371-L391.
[http://dx.doi.org/10.1152/ajplung.00486.2016] [PMID: 28062486]
[33]
McNeil, P.L.; Ito, S. Gastrointestinal cell plasma membrane wounding and resealing in vivo. Gastroenterology, 1989, 96(5 Pt 1), 1238-1248.
[http://dx.doi.org/10.1016/S0016-5085(89)80010-1] [PMID: 2703112]
[34]
Proske, U.; Morgan, D.L. Muscle damage from eccentric exercise: mechanism, mechanical signs, adaptation and clinical applications. J. Physiol., 2001, 537(Pt 2), 333-345.
[http://dx.doi.org/10.1111/j.1469-7793.2001.00333.x] [PMID: 11731568]
[35]
Fridén, J.; Sjöström, M.; Ekblom, B. Myofibrillar damage following intense eccentric exercise in man. Int. J. Sports Med., 1983, 4(3), 170-176.
[http://dx.doi.org/10.1055/s-2008-1026030] [PMID: 6629599]
[36]
Tidball, J.G. Mechanisms of muscle injury, repair, and regeneration. Compr. Physiol., 2011, 1(4), 2029-2062.
[http://dx.doi.org/10.1002/cphy.c100092] [PMID: 23733696]
[37]
Shin, J.; Tajrishi, M.M.; Ogura, Y.; Kumar, A. Wasting mechanisms in muscular dystrophy. Int. J. Biochem. Cell Biol., 2013, 45(10), 2266-2279.
[http://dx.doi.org/10.1016/j.biocel.2013.05.001] [PMID: 23669245]
[38]
Potez, S.; Luginbühl, M.; Monastyrskaya, K.; Hostettler, A.; Draeger, A.; Babiychuk, E.B. Tailored protection against plasmalemmal injury by annexins with different Ca2+ sensitivities. J. Biol. Chem., 2011, 286(20), 17982-17991.
[http://dx.doi.org/10.1074/jbc.M110.187625] [PMID: 21454475]
[39]
Weng, X.; Luecke, H.; Song, I.S.; Kang, D.S.; Kim, S.H.; Huber, R. Crystal structure of human annexin I at 2.5 A resolution. Protein Sci., 1993, 2(3), 448-458.
[http://dx.doi.org/10.1002/pro.5560020317] [PMID: 8453382]
[40]
Bharadwaj, A.; Bydoun, M.; Holloway, R.; Waisman, D. Annexin A2 heterotetramer: structure and function. Int. J. Mol. Sci., 2013, 14(3), 6259-6305.
[http://dx.doi.org/10.3390/ijms14036259] [PMID: 23519104]
[41]
Lennon, N.J.; Kho, A.; Bacskai, B.J.; Perlmutter, S.L.; Hyman, B.T.; Brown, R.H., Jr Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing. J. Biol. Chem., 2003, 278(50), 50466-50473.
[http://dx.doi.org/10.1074/jbc.M307247200] [PMID: 14506282]
[42]
McNeil, A.K.; Rescher, U.; Gerke, V.; McNeil, P.L. Requirement for annexin A1 in plasma membrane repair. J. Biol. Chem., 2006, 281(46), 35202-35207.
[http://dx.doi.org/10.1074/jbc.M606406200] [PMID: 16984915]
[43]
Babiychuk, E.B.; Monastyrskaya, K.; Potez, S.; Draeger, A. Blebbing confers resistance against cell lysis. Cell Death Differ., 2011, 18(1), 80-89.
[http://dx.doi.org/10.1038/cdd.2010.81] [PMID: 20596076]
[44]
Swaggart, K.A.; Demonbreun, A.R.; Vo, A.H.; Swanson, K.E.; Kim, E.Y.; Fahrenbach, J.P.; Holley-Cuthrell, J.; Eskin, A.; Chen, Z.; Squire, K.; Heydemann, A.; Palmer, A.A.; Nelson, S.F.; McNally, E.M. Annexin A6 modifies muscular dystrophy by mediating sarcolemmal repair. Proc. Natl. Acad. Sci. USA, 2014, 111(16), 6004-6009.
[http://dx.doi.org/10.1073/pnas.1324242111] [PMID: 24717843]
[45]
Jaiswal, J.K.; Lauritzen, S.P.; Scheffer, L.; Sakaguchi, M.; Bunkenborg, J.; Simon, S.M.; Kallunki, T.; Jäättelä, M.; Nylandsted, J. S100A11 is required for efficient plasma membrane repair and survival of invasive cancer cells. Nat. Commun., 2014, 5, 3795.
[http://dx.doi.org/10.1038/ncomms4795] [PMID: 24806074]
[46]
Jaiswal, J.K.; Nylandsted, J. S100 and annexin proteins identify cell membrane damage as the Achilles heel of metastatic cancer cells. Cell Cycle, 2015, 14(4), 502-509.
[http://dx.doi.org/10.1080/15384101.2014.995495] [PMID: 25565331]
[47]
Rafn, B.; Nielsen, C.F.; Andersen, S.H.; Szyniarowski, P.; Corcelle-Termeau, E.; Valo, E.; Fehrenbacher, N.; Olsen, C.J.; Daugaard, M.; Egebjerg, C.; Bøttzauw, T.; Kohonen, P.; Nylandsted, J.; Hautaniemi, S.; Moreira, J.; Jäättelä, M.; Kallunki, T. ErbB2-driven breast cancer cell invasion depends on a complex signaling network activating myeloid zinc finger-1-dependent cathepsin B expression. Mol. Cell, 2012, 45(6), 764-776.
[http://dx.doi.org/10.1016/j.molcel.2012.01.029] [PMID: 22464443]
[48]
Egeblad, M.; Mortensen, O.H.; Jäättelä, M. Truncated ErbB2 receptor enhances ErbB1 signaling and induces reversible, ERK-independent loss of epithelial morphology. Int. J. Cancer, 2001, 94(2), 185-191.
[http://dx.doi.org/10.1002/ijc.1459] [PMID: 11668496]
[49]
Mussunoor, S.; Murray, G.I. The role of annexins in tumour development and progression. J. Pathol., 2008, 216(2), 131-140.
[http://dx.doi.org/10.1002/path.2400] [PMID: 18698663]
[50]
Rehman, I.; Azzouzi, A.R.; Cross, S.S.; Deloulme, J.C.; Catto, J.W.; Wylde, N.; Larre, S.; Champigneuille, J.; Hamdy, F.C. Dysregulated expression of S100A11 (calgizzarin) in prostate cancer and precursor lesions. Hum. Pathol., 2004, 35(11), 1385-1391.
[http://dx.doi.org/10.1016/j.humpath.2004.07.015] [PMID: 15668896]
[51]
Xiao, M.B.; Jiang, F.; Ni, W.K.; Chen, B.Y.; Lu, C.H.; Li, X.Y.; Ni, R.Z. High expression of S100A11 in pancreatic adenocarcinoma is an unfavorable prognostic marker. Med. Oncol., 2012, 29(3), 1886-1891.
[http://dx.doi.org/10.1007/s12032-011-0058-y] [PMID: 21912994]
[52]
Liu, X.; Ma, D.; Jing, X.; Wang, B.; Yang, W.; Qiu, W. Overexpression of ANXA2 predicts adverse outcomes of patients with malignant tumors: a systematic review and meta-analysis. Med. Oncol., 2015, 32(1), 392.
[http://dx.doi.org/10.1007/s12032-014-0392-y] [PMID: 25476478]
[53]
Grewal, T.; Enrich, C. Annexins--modulators of EGF receptor signalling and trafficking. Cell. Signal., 2009, 21(6), 847-858.
[http://dx.doi.org/10.1016/j.cellsig.2009.01.031] [PMID: 19385045]
[54]
Qi, H.; Liu, S.; Guo, C.; Wang, J.; Greenaway, F.T.; Sun, M.Z. Role of annexin A6 in cancer. Oncol. Lett., 2015, 10(4), 1947-1952.
[http://dx.doi.org/10.3892/ol.2015.3498] [PMID: 26622779]
[55]
Hannon, R.; Croxtall, J.D.; Getting, S.J.; Roviezzo, F.; Yona, S.; Paul-Clark, M.J.; Gavins, F.N.; Perretti, M.; Morris, J.F.; Buckingham, J.C.; Flower, R.J. Aberrant inflammation and resistance to glucocorticoids in annexin 1-/- mouse. FASEB J., 2003, 17(2), 253-255.
[http://dx.doi.org/10.1096/fj.02-0239fje] [PMID: 12475898]
[56]
Boye, T.L.; Maeda, K.; Pezeshkian, W.; Sønder, S.L.; Haeger, S.C.; Gerke, V.; Simonsen, A.C.; Nylandsted, J. Annexin A4 and A6 induce membrane curvature and constriction during cell membrane repair. Nat. Commun., 2017, 8(1), 1623.
[http://dx.doi.org/10.1038/s41467-017-01743-6] [PMID: 29158488]
[57]
Idone, V.; Tam, C.; Goss, J.W.; Toomre, D.; Pypaert, M.; Andrews, N.W. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis. J. Cell Biol., 2008, 180(5), 905-914.
[http://dx.doi.org/10.1083/jcb.200708010] [PMID: 18316410]
[58]
Idone, V.; Tam, C.; Andrews, N.W. Two-way traffic on the road to plasma membrane repair. Trends Cell Biol., 2008, 18(11), 552-559.
[http://dx.doi.org/10.1016/j.tcb.2008.09.001] [PMID: 18848451]
[59]
Steinhardt, R.A.; Bi, G.; Alderton, J.M. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release. Science, 1994, 263(5145), 390-393.
[http://dx.doi.org/10.1126/science.7904084] [PMID: 7904084]
[60]
Jimenez, A.J.; Maiuri, P.; Lafaurie-Janvore, J.; Divoux, S.; Piel, M.; Perez, F. ESCRT machinery is required for plasma membrane repair. Science, 2014, 343(6174)1247136
[http://dx.doi.org/10.1126/science.1247136] [PMID: 24482116]
[61]
Scheffer, L.L.; Sreetama, S.C.; Sharma, N.; Medikayala, S.; Brown, K.J.; Defour, A.; Jaiswal, J.K. Mechanism of Ca2+-triggered ESCRT assembly and regulation of cell membrane repair. Nat. Commun., 2014, 5, 5646.
[http://dx.doi.org/10.1038/ncomms6646] [PMID: 25534348]
[62]
Bement, W.M.; Mandato, C.A.; Kirsch, M.N. Wound-induced assembly and closure of an actomyosin purse string in Xenopus oocytes. Curr. Biol., 1999, 9(11), 579-587.
[http://dx.doi.org/10.1016/S0960-9822(99)80261-9] [PMID: 10359696]
[63]
Seemann, J.; Weber, K.; Gerke, V. Annexin I targets S100C to early endosomes. FEBS Lett., 1997, 413(1), 185-190.
[http://dx.doi.org/10.1016/S0014-5793(97)00911-3] [PMID: 9287141]
[64]
Rescher, U.; Zobiack, N.; Gerke, V. Intact Ca(2+)-binding sites are required for targeting of annexin 1 to endosomal membranes in living HeLa cells. J. Cell Sci., 2000, 113(Pt 22), 3931-3938.
[PMID: 11058080]
[65]
König, J.; Gerke, V. Modes of annexin-membrane interactions analyzed by employing chimeric annexin proteins. Biochim. Biophys. Acta, 2000, 1498(2-3), 174-180.
[http://dx.doi.org/10.1016/S0167-4889(00)00094-X] [PMID: 11108961]
[66]
Harder, T.; Gerke, V. The subcellular distribution of early endosomes is affected by the annexin II2p11(2) complex. J. Cell Biol., 1993, 123(5), 1119-1132.
[http://dx.doi.org/10.1083/jcb.123.5.1119] [PMID: 8245122]
[67]
Salzer, U.; Hinterdorfer, P.; Hunger, U.; Borken, C.; Prohaska, R. Ca(++)-dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, synexin (annexin VII), and sorcin. Blood, 2002, 99(7), 2569-2577.
[http://dx.doi.org/10.1182/blood.V99.7.2569] [PMID: 11895795]
[68]
Karatekin, E.; Sandre, O.; Guitouni, H.; Borghi, N.; Puech, P.H.; Brochard-Wyart, F. Cascades of transient pores in giant vesicles: line tension and transport. Biophys. J., 2003, 84(3), 1734-1749.
[http://dx.doi.org/10.1016/S0006-3495(03)74981-9] [PMID: 12609875]
[69]
Chabanon, M.; Ho, J.C.S.; Liedberg, B.; Parikh, A.N.; Rangamani, P. Pulsatile lipid vesicles under osmotic stress. Biophys. J., 2017, 112(8), 1682-1691.
[http://dx.doi.org/10.1016/j.bpj.2017.03.018] [PMID: 28445759]
[70]
Simonsen, A.C. Activation of phospholipase A2 by ternary model membranes. Biophys. J., 2008, 94(10), 3966-3975.
[http://dx.doi.org/10.1529/biophysj.107.114363] [PMID: 18234820]
[71]
Jensen, M.H.; Morris, E.J.; Simonsen, A.C. Domain shapes, coarsening, and random patterns in ternary membranes. Langmuir, 2007, 23(15), 8135-8141.
[http://dx.doi.org/10.1021/la700647v] [PMID: 17590026]
[72]
Simonsen, A.C.; Bagatolli, L.A. Structure of spin-coated lipid films and domain formation in supported membranes formed by hydration. Langmuir, 2004, 20(22), 9720-9728.
[http://dx.doi.org/10.1021/la048683+] [PMID: 15491207]
[73]
Nielsen, M.M.; Simonsen, A.C. Imaging ellipsometry of spin-coated membranes: mapping of multilamellar films, hydrated membranes, and fluid domains. Langmuir, 2013, 29(5), 1525-1532.
[http://dx.doi.org/10.1021/la3046675] [PMID: 23281595]
[74]
Hakobyan, D.; Gerke, V.; Heuer, A. Modeling of annexin A2-Membrane interactions by molecular dynamics simulations. PLoS One, 2017, 12(9)e0185440
[http://dx.doi.org/10.1371/journal.pone.0185440] [PMID: 28937994]
[75]
Boye, T.L.; Jeppesen, J.C.; Maeda, K.; Pezeshkian, W.; Solovyeva, V.; Nylandsted, J.; Simonsen, A.C. Annexins induce curvature on free-edge membranes displaying distinct morphologies. Sci. Rep., 2018, 8(1), 10309.
[http://dx.doi.org/10.1038/s41598-018-28481-z] [PMID: 29985397]
[76]
Piljic, A.; Schultz, C. Annexin A4 self-association modulates general membrane protein mobility in living cells. Mol. Biol. Cell, 2006, 17(7), 3318-3328.
[http://dx.doi.org/10.1091/mbc.e06-01-0041] [PMID: 16687573]
[77]
Bouter, A.; Gounou, C.; Bérat, R.; Tan, S.; Gallois, B.; Granier, T.; d’Estaintot, B.L.; Pöschl, E.; Brachvogel, B.; Brisson, A.R. Annexin-A5 assembled into two-dimensional arrays promotes cell membrane repair. Nat. Commun., 2011, 2, 270.
[http://dx.doi.org/10.1038/ncomms1270] [PMID: 21468022]
[78]
Huber, R.; Römisch, J.; Paques, E.P. The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes. EMBO J., 1990, 9(12), 3867-3874.
[http://dx.doi.org/10.1002/j.1460-2075.1990.tb07605.x] [PMID: 2147412]
[79]
Koopman, G.; Reutelingsperger, C.P.; Kuijten, G.A.; Keehnen, R.M.; Pals, S.T.; van Oers, M.H. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood, 1994, 84(5), 1415-1420.
[http://dx.doi.org/10.1182/blood.V84.5.1415.bloodjournal8451415] [PMID: 8068938]
[80]
Zhang, G.; Gurtu, V.; Kain, S.R.; Yan, G. Early detection of apoptosis using a fluorescent conjugate of annexin V. Biotechniques, 1997, 23(3), 525-531.
[http://dx.doi.org/10.2144/97233pf01] [PMID: 9298227]
[81]
Bouter, A.; Carmeille, R.; Gounou, C.; Bouvet, F.; Degrelle, S.A.; Evain-Brion, D.; Brisson, A.R. Review: Annexin-A5 and cell membrane repair. Placenta, 2015, 36(Suppl. 1), S43-S49.
[http://dx.doi.org/10.1016/j.placenta.2015.01.193] [PMID: 25701430]
[82]
Carmeille, R.; Bouvet, F.; Tan, S.; Croissant, C.; Gounou, C.; Mamchaoui, K.; Mouly, V.; Brisson, A.R.; Bouter, A. Membrane repair of human skeletal muscle cells requires Annexin-A5. Biochim. Biophys. Acta, 2016, 1863(9), 2267-2279.
[http://dx.doi.org/10.1016/j.bbamcr.2016.06.003] [PMID: 27286750]
[83]
Carmeille, R.; Degrelle, S.A.; Plawinski, L.; Bouvet, F.; Gounou, C.; Evain-Brion, D.; Brisson, A.R.; Bouter, A. Annexin-A5 promotes membrane resealing in human trophoblasts. Biochim. Biophys. Acta, 2015, 1853(9), 2033-2044.
[http://dx.doi.org/10.1016/j.bbamcr.2014.12.038] [PMID: 25595530]
[84]
Gerke, V.; Weber, K. Identity of p36K phosphorylated upon Rous sarcoma virus transformation with a protein purified from brush borders; calcium-dependent binding to non-erythroid spectrin and F-actin. EMBO J., 1984, 3(1), 227-233.
[http://dx.doi.org/10.1002/j.1460-2075.1984.tb01789.x] [PMID: 6323166]
[85]
Zaks, W.J.; Creutz, C.E. Ca(2+)-dependent annexin self-association on membrane surfaces. Biochemistry, 1991, 30(40), 9607-9615.
[http://dx.doi.org/10.1021/bi00104a007] [PMID: 1911746]
[86]
Zanotti, G.; Malpeli, G.; Gliubich, F.; Folli, C.; Stoppini, M.; Olivi, L.; Savoia, A.; Berni, R. Structure of the trigonal crystal form of bovine annexin IV. Biochem. J., 1998, 329(Pt 1), 101-106.
[http://dx.doi.org/10.1042/bj3290101] [PMID: 9405281]
[87]
Kaetzel, M.A.; Mo, Y.D.; Mealy, T.R.; Campos, B.; Bergsma-Schutter, W.; Brisson, A.; Dedman, J.R.; Seaton, B.A. Phosphorylation mutants elucidate the mechanism of annexin IV-mediated membrane aggregation. Biochemistry, 2001, 40(13), 4192-4199.
[http://dx.doi.org/10.1021/bi002507s] [PMID: 11300800]
[88]
Frislev, H.S.; Boye, T.L.; Nylandsted, J.; Otzen, D. Liprotides kill cancer cells by disrupting the plasma membrane. Sci. Rep., 2017, 7(1), 15129.
[http://dx.doi.org/10.1038/s41598-017-15003-6] [PMID: 29123177]
[89]
Choi, C.H.; Chung, J.Y.; Chung, E.J.; Sears, J.D.; Lee, J.W.; Bae, D.S.; Hewitt, S.M. Prognostic significance of annexin A2 and annexin A4 expression in patients with cervical cancer. BMC Cancer, 2016, 16, 448.
[http://dx.doi.org/10.1186/s12885-016-2459-y] [PMID: 27402115]
[90]
Lokman, N.A.; Ween, M.P.; Oehler, M.K.; Ricciardelli, C. The role of annexin A2 in tumorigenesis and cancer progression. Cancer Microenviron., 2011, 4(2), 199-208.
[http://dx.doi.org/10.1007/s12307-011-0064-9] [PMID: 21909879]
[91]
Sobral-Leite, M.; Wesseling, J.; Smit, V.T.; Nevanlinna, H.; van Miltenburg, M.H.; Sanders, J.; Hofland, I.; Blows, F.M.; Coulson, P.; Patrycja, G.; Schellens, J.H.; Fagerholm, R.; Heikkilä, P.; Aittomäki, K.; Blomqvist, C.; Provenzano, E.; Ali, H.R.; Figueroa, J.; Sherman, M.; Lissowska, J.; Mannermaa, A.; Kataja, V.; Kosma, V.M.; Hartikainen, J.M.; Phillips, K.A.; Couch, F.J.; Olson, J.E.; Vachon, C.; Visscher, D.; Brenner, H.; Butterbach, K.; Arndt, V.; Holleczek, B.; Hooning, M.J.; Hollestelle, A.; Martens, J.W.; van Deurzen, C.H.; van de Water, B.; Broeks, A.; Chang-Claude, J.; Chenevix-Trench, G.; Easton, D.F.; Pharoah, P.D.; García-Closas, M.; de Graauw, M.; Schmidt, M.K. kConFab/AOCS Investigators. Annexin A1 expression in a pooled breast cancer series: association with tumor subtypes and prognosis. BMC Med., 2015, 13, 156.
[http://dx.doi.org/10.1186/s12916-015-0392-6] [PMID: 26137966]
[92]
Yao, H.; Zhang, Z.; Xiao, Z.; Chen, Y.; Li, C.; Zhang, P.; Li, M.; Liu, Y.; Guan, Y.; Yu, Y.; Chen, Z. Identification of metastasis associated proteins in human lung squamous carcinoma using two-dimensional difference gel electrophoresis and laser capture microdissection. Lung Cancer, 2009, 65(1), 41-48.
[http://dx.doi.org/10.1016/j.lungcan.2008.10.024] [PMID: 19058872]
[93]
Yan, X.; Yin, J.; Yao, H.; Mao, N.; Yang, Y.; Pan, L. Increased expression of annexin A3 is a mechanism of platinum resistance in ovarian cancer. Cancer Res., 2010, 70(4), 1616-1624.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-3215] [PMID: 20103635]
[94]
Kim, A.; Enomoto, T.; Serada, S.; Ueda, Y.; Takahashi, T.; Ripley, B.; Miyatake, T.; Fujita, M.; Lee, C.M.; Morimoto, K.; Fujimoto, M.; Kimura, T.; Naka, T. Enhanced expression of Annexin A4 in clear cell carcinoma of the ovary and its association with chemoresistance to carboplatin. Int. J. Cancer, 2009, 125(10), 2316-2322.
[http://dx.doi.org/10.1002/ijc.24587] [PMID: 19598262]
[95]
Ma, R.L.; Shen, L.Y.; Chen, K.N. Coexpression of ANXA2, SOD2 and HOXA13 predicts poor prognosis of esophageal squamous cell carcinoma. Oncol. Rep., 2014, 31(5), 2157-2164.
[http://dx.doi.org/10.3892/or.2014.3088] [PMID: 24626613]
[96]
Yang, S.F.; Hsu, H.L.; Chao, T.K.; Hsiao, C.J.; Lin, Y.F.; Cheng, C.W. Annexin A2 in renal cell carcinoma: expression, function, and prognostic significance. Urol. Oncol., 2015, 33(1), 22.e11-22.e21.
[http://dx.doi.org/10.1016/j.urolonc.2014.08.015] [PMID: 25284003]
[97]
Wang, Y.S.; Li, H.; Li, Y.; Zhu, H.; Jin, Y.H. Identification of natural compounds targeting Annexin A2 with an anti-cancer effect. Protein Cell, 2018, 9(6), 568-579.
[http://dx.doi.org/10.1007/s13238-018-0513-z] [PMID: 29508276]
[98]
Attele, A.S.; Wu, J.A.; Yuan, C.S. Ginseng pharmacology: multiple constituents and multiple actions. Biochem. Pharmacol., 1999, 58(11), 1685-1693.
[http://dx.doi.org/10.1016/S0006-2952(99)00212-9] [PMID: 10571242]
[99]
Reddy, T.R.; Li, C.; Guo, X.; Fischer, P.M.; Dekker, L.V. Design, synthesis and SAR exploration of tri-substituted 1,2,4-triazoles as inhibitors of the annexin A2-S100A10 protein interaction. Bioorg. Med. Chem., 2014, 22(19), 5378-5391.
[http://dx.doi.org/10.1016/j.bmc.2014.07.043] [PMID: 25172147]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy