1hm6 Citations

X-ray structure of full-length annexin 1 and implications for membrane aggregation.

J Mol Biol 306 489-98 (2001)
Cited: 94 times
EuropePMC logo PMID: 11178908

Abstract

Annexins comprise a multigene family of Ca2+ and phospholipid- binding proteins. They consist of a conserved C-terminal or core domain that confers Ca2+-dependent phospholipid binding and an N-terminal domain that is variable in sequence and length and responsible for the specific properties of each annexin. Crystal structures of various annexin core domains have revealed a high degree of similarity. From these and other studies it is evident that the core domain harbors the calcium-binding sites that interact with the phospholipid headgroups. However, no structure has been reported of an annexin with a complete N-terminal domain. We have now solved the crystal structure of such a full-length annexin, annexin 1. Annexin 1 is active in membrane aggregation and its refined 1.8 A structure shows an alpha-helical N-terminal domain connected to the core domain by a flexible linker. It is surprising that the two alpha-helices present in the N-terminal domain of 41 residues interact intimately with the core domain, with the amphipathic helix 2-12 of the N-terminal domain replacing helix D of repeat III of the core. In turn, helix D is unwound into a flap now partially covering the N-terminal helix. Implications for membrane aggregation will be discussed and a model of aggregation based on the structure will be presented.

Articles - 1hm6 mentioned but not cited (14)

  1. Annexin-phospholipid interactions. Functional implications. Lizarbe MA, Barrasa JI, Olmo N, Gavilanes F, Turnay J. Int J Mol Sci 14 2652-2683 (2013)
  2. A calcium-driven conformational switch of the N-terminal and core domains of annexin A1. Rosengarth A, Luecke H. J Mol Biol 326 1317-1325 (2003)
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  7. Structure-function relationship in annexin A13, the founder member of the vertebrate family of annexins. Turnay J, Lecona E, Fernández-Lizarbe S, Guzmán-Aránguez A, Fernández MP, Olmo N, Lizarbe MA. Biochem J 389 899-911 (2005)
  8. The underlying molecular mechanism and potential drugs for treatment in papillary renal cell carcinoma: A study based on TCGA and Cmap datasets. Pang JS, Li ZK, Lin P, Wang XD, Chen G, Yan HB, Li SH. Oncol Rep 41 2089-2102 (2019)
  9. Overcoming the blood-brain barrier by Annexin A1-binding peptide to target brain tumours. Nonaka M, Suzuki-Anekoji M, Nakayama J, Mabashi-Asazuma H, Jarvis DL, Yeh JC, Yamasaki K, Akama TO, Huang CT, Campos AR, Nagaoka M, Sasai T, Kimura-Takagi I, Suwa Y, Yaegashi T, Shibata TK, Sugihara K, Nishizawa-Harada C, Fukuda M, Fukuda MN. Br J Cancer 123 1633-1643 (2020)
  10. Inhibition of Triple-Negative Breast Cancer Cell Aggressiveness by Cathepsin D Blockage: Role of Annexin A1. Zóia MAP, Azevedo FVP, Vecchi L, Mota STS, Rodovalho VR, Cordeiro AO, Correia LIV, Silva ACA, Ávila VMR, Araújo TG, Goulart LR. Int J Mol Sci 20 E1337 (2019)
  11. Deciphering potential pharmacological mechanism of Sha-Shen-Mai-Dong decoction on primary Sjogren's syndrome. Jiang Y, Zhao X, Yu J, Wang Q, Wen C, Huang L. BMC Complement Med Ther 21 79 (2021)
  12. HDX-MS for Epitope Characterization of a Therapeutic ANTIBODY Candidate on the Calcium-Binding Protein Annexin-A1. Gramlich M, Hays HCW, Crichton S, Kaiser PD, Heine A, Schneiderhan-Marra N, Rothbauer U, Stoll D, Maier S, Zeck A. Antibodies (Basel) 10 11 (2021)
  13. Development of an orally-administrable tumor vasculature-targeting therapeutic using annexin A1-binding D-peptides. Nonaka M, Mabashi-Asazuma H, Jarvis DL, Yamasaki K, Akama TO, Nagaoka M, Sasai T, Kimura-Takagi I, Suwa Y, Yaegashi T, Huang CT, Nishizawa-Harada C, Fukuda MN. PLoS One 16 e0241157 (2021)
  14. Nudged Elastic Band Study on the N-Terminal Domain Conformational Pathways of Annexin A1 from a Buried State to an Exposed State. Lewis K, Lindsay S, Li Y. J Phys Chem B 123 10163-10170 (2019)


Reviews citing this publication (25)

  1. Annexins: from structure to function. Gerke V, Moss SE. Physiol Rev 82 331-371 (2002)
  2. Annexin 1: the new face of an old molecule. Lim LH, Pervaiz S. FASEB J 21 968-975 (2007)
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  14. S100-annexin complexes--structural insights. Rintala-Dempsey AC, Rezvanpour A, Shaw GS. FEBS J 275 4956-4966 (2008)
  15. Expression and functions of annexins in the kidney. Markoff A, Gerke V. Am J Physiol Renal Physiol 289 F949-56 (2005)
  16. A twist in anti-inflammation: annexin 1 acts via the lipoxin A4 receptor. Gavins FN, Sawmynaden P, Chatterjee BE, Perretti M. Prostaglandins Leukot Essent Fatty Acids 73 211-219 (2005)
  17. Annexins as Overlooked Regulators of Membrane Trafficking in Plant Cells. Konopka-Postupolska D, Clark G. Int J Mol Sci 18 E863 (2017)
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  19. Annexin A1 influences in breast cancer: Controversies on contributions to tumour, host and immunoediting processes. Tu Y, Johnstone CN, Stewart AG. Pharmacol Res 119 278-288 (2017)
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  22. Annexins in Influenza Virus Replication and Pathogenesis. Ampomah PB, Kong WT, Zharkova O, Chua SCJH, Perumal Samy R, Lim LHK. Front Pharmacol 9 1282 (2018)
  23. From NSAIDs to Glucocorticoids and Beyond. Sinniah A, Yazid S, Flower RJ. Cells 10 3524 (2021)
  24. Annexin A protein family: Focusing on the occurrence, progression and treatment of cancer. Zhang H, Zhang Z, Guo T, Chen G, Liu G, Song Q, Li G, Xu F, Dong X, Yang F, Cao C, Zhong D, Li S, Li Y, Wang M, Li B, Yang L. Front Cell Dev Biol 11 1141331 (2023)
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Articles citing this publication (55)

  1. Annexin A1: a central player in the anti-inflammatory and neuroprotective role of microglia. McArthur S, McArthur S, Cristante E, Paterno M, Christian H, Roncaroli F, Gillies GE, Solito E. J Immunol 185 6317-6328 (2010)
  2. Macrophage surface expression of annexins I and II in the phagocytosis of apoptotic lymphocytes. Fan X, Krahling S, Smith D, Williamson P, Schlegel RA. Mol Biol Cell 15 2863-2872 (2004)
  3. Annexin A1 and the regulation of innate and adaptive immunity. Gavins FN, Hickey MJ. Front Immunol 3 354 (2012)
  4. Annexin A1 interaction with the FPR2/ALX receptor: identification of distinct domains and downstream associated signaling. Bena S, Brancaleone V, Wang JM, Perretti M, Flower RJ. J Biol Chem 287 24690-24697 (2012)
  5. Anti-inflammatory effects of annexin-1: stimulation of IL-10 release and inhibition of nitric oxide synthesis. Ferlazzo V, D'Agostino P, Milano S, Caruso R, Feo S, Cillari E, Parente L. Int Immunopharmacol 3 1363-1369 (2003)
  6. Annexin A1 released from apoptotic cells acts through formyl peptide receptors to dampen inflammatory monocyte activation via JAK/STAT/SOCS signalling. Pupjalis D, Goetsch J, Kottas DJ, Gerke V, Rescher U. EMBO Mol Med 3 102-114 (2011)
  7. Lipid segregation and membrane budding induced by the peripheral membrane binding protein annexin A2. Drücker P, Pejic M, Galla HJ, Gerke V. J Biol Chem 288 24764-24776 (2013)
  8. Proteolytic cleavage of annexin 1 by human leukocyte elastase. Rescher U, Goebeler V, Wilbers A, Gerke V. Biochim Biophys Acta 1763 1320-1324 (2006)
  9. Evidence for an anti-inflammatory loop centered on polymorphonuclear leukocyte formyl peptide receptor 2/lipoxin A4 receptor and operative in the inflamed microvasculature. Brancaleone V, Dalli J, Bena S, Flower RJ, Cirino G, Perretti M. J Immunol 186 4905-4914 (2011)
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  11. Annexin A1 May Induce Pancreatic Cancer Progression as a Key Player of Extracellular Vesicles Effects as Evidenced in the In Vitro MIA PaCa-2 Model System. Pessolano E, Belvedere R, Bizzarro V, Franco P, Marco I, Porta A, Tosco A, Parente L, Perretti M, Petrella A. Int J Mol Sci 19 E3878 (2018)
  12. Identification of annexin A1 as a novel substrate for E6AP-mediated ubiquitylation. Shimoji T, Murakami K, Sugiyama Y, Matsuda M, Inubushi S, Nasu J, Shirakura M, Suzuki T, Wakita T, Kishino T, Hotta H, Miyamura T, Shoji I. J Cell Biochem 106 1123-1135 (2009)
  13. The S100A10-annexin A2 complex provides a novel asymmetric platform for membrane repair. Rezvanpour A, Santamaria-Kisiel L, Shaw GS. J Biol Chem 286 40174-40183 (2011)
  14. Annexin A1 attenuates microvascular complications through restoration of Akt signalling in a murine model of type 1 diabetes. Purvis GSD, Chiazza F, Chen J, Azevedo-Loiola R, Martin L, Kusters DHM, Reutelingsperger C, Fountoulakis N, Gnudi L, Yaqoob MM, Collino M, Thiemermann C, Solito E. Diabetologia 61 482-495 (2018)
  15. Phosphorylation of annexin A1 by TRPM7 kinase: a switch regulating the induction of an α-helix. Dorovkov MV, Kostyukova AS, Ryazanov AG. Biochemistry 50 2187-2193 (2011)
  16. Annexin-A6 presents two modes of association with phospholipid membranes. A combined QCM-D, AFM and cryo-TEM study. Buzhynskyy N, Golczak M, Lai-Kee-Him J, Lambert O, Tessier B, Gounou C, Bérat R, Simon A, Granier T, Chevalier JM, Mazères S, Bandorowicz-Pikula J, Pikula S, Brisson AR. J Struct Biol 168 107-116 (2009)
  17. Annexin-1 regulated by HAUSP is essential for UV-induced damage response. Park JJ, Lim KH, Baek KH. Cell Death Dis 6 e1654 (2015)
  18. Nuclear translocation of annexin 1 following oxygen-glucose deprivation-reperfusion induces apoptosis by regulating Bid expression via p53 binding. Li X, Zhao Y, Xia Q, Zheng L, Liu L, Zhao B, Shi J. Cell Death Dis 7 e2356 (2016)
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  21. The annexin I sequence gln(9)-ala(10)-trp(11)-phe(12) is a core structure for interaction with the formyl peptide receptor 1. Movitz C, Brive L, Hellstrand K, Rabiet MJ, Dahlgren C. J Biol Chem 285 14338-14345 (2010)
  22. Ca(2+) and membrane binding to annexin 3 modulate the structure and dynamics of its N terminus and domain III. Sopkova J, Raguenes-Nicol C, Vincent M, Chevalier A, Lewit-Bentley A, Russo-Marie F, Gallay J. Protein Sci 11 1613-1625 (2002)
  23. Characterization of pro-invasive mechanisms and N-terminal cleavage of ANXA1 in melanoma. Boudhraa Z, Merle C, Mazzocut D, Chezal JM, Chambon C, Miot-Noirault E, Theisen M, Bouchon B, Degoul F. Arch Dermatol Res 306 903-914 (2014)
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  33. Partial truncation of the NH2-terminus affects physical characteristics and membrane binding, aggregation, and fusion properties of annexin A7. Naidu DG, Raha A, Chen XL, Spitzer AR, Chander A. Biochim Biophys Acta 1734 152-168 (2005)
  34. Annexin A7 trafficking to alveolar type II cell surface: possible roles for protein insertion into membranes and lamellar body secretion. Chander A, Gerelsaikhan T, Vasa PK, Holbrook K. Biochim Biophys Acta 1833 1244-1255 (2013)
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  39. Partially reversible adsorption of annexin A1 on POPC/POPS bilayers investigated by QCM measurements, SFM, and DMC simulations. Kastl K, Menke M, Lüthgens E, Faiss S, Gerke V, Janshoff A, Steinem C. Chembiochem 7 106-115 (2006)
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  41. The crystal structure of annexin A8 is similar to that of annexin A3. Réty S, Sopková-de Oliveira Santos J, Dreyfuss L, Blondeau K, Hofbauerová K, Raguénès-Nicol C, Kerboeuf D, Renouard M, Russo-Marie F, Lewit-Bentley A. J Mol Biol 345 1131-1139 (2005)
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  46. Annexin A1 accounts for an anti-inflammatory binding target of sesamin metabolites. Kabe Y, Takemoto D, Kanai A, Hirai M, Ono Y, Akazawa S, Horikawa M, Kitagawa Y, Handa H, Rogi T, Shibata H, Suematsu M. NPJ Sci Food 4 4 (2020)
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  49. Upregulation of annexin A1 protein expression in the intratumoral vasculature of human non-small-cell lung carcinoma and rodent tumor models. Allen KL, Cann J, Zhao W, Peterson N, Lazzaro M, Zhong H, Wu H, Dall'Acqua WF, Borrok MJ, Damschroder MM, Tsui P, Li Q. PLoS One 15 e0234268 (2020)
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Related citations provided by authors (1)

  1. Crystallization and Preliminary X-ray Analysis of Full-length Annexin I Comprising the Core and N-terminal Domain.. Rosengarth A, Luecke H Acta Crystallogr. D Biol. Crystallogr. 56 1459-1461 (2000)