6tql › Citations

Cryo-EM structure of native human uromodulin, a zona pellucida module polymer.

Figure EV1
Figure 1
Figure EV2
Stsiapanava A, Xu C, Brunati M, Zamora-Caballero S, Schaeffer C, Bokhove M, Han L, Hebert H, Carroni M, Yasumasu S, Rampoldi L, Wu B, Jovine L
OpenAccess logo EMBO J 39 e106807 (2020)
Related entries: 3nk3, 3nk4, 4wrn, 5bup, 6tqk

Cited: 18 times
EuropePMC logo PMID: 33196145

Abstract

Assembly of extracellular filaments and matrices mediating fundamental biological processes such as morphogenesis, hearing, fertilization, and antibacterial defense is driven by a ubiquitous polymerization module known as zona pellucida (ZP) "domain". Despite the conservation of this element from hydra to humans, no detailed information is available on the filamentous conformation of any ZP module protein. Here, we report a cryo-electron microscopy study of uromodulin (UMOD)/Tamm-Horsfall protein, the most abundant protein in human urine and an archetypal ZP module-containing molecule, in its mature homopolymeric state. UMOD forms a one-start helix with an unprecedented 180-degree twist between subunits enfolded by interdomain linkers that have completely reorganized as a result of propeptide dissociation. Lateral interaction between filaments in the urine generates sheets exposing a checkerboard of binding sites to capture uropathogenic bacteria, and UMOD-based models of heteromeric vertebrate egg coat filaments identify a common sperm-binding region at the interface between subunits.

Reviews citing this publication (8)

  1. Find and fuse: Unsolved mysteries in sperm-egg recognition. Bianchi E, Wright GJ. PLoS Biol 18 e3000953 (2020)
  2. Zona Pellucida Genes and Proteins: Essential Players in Mammalian Oogenesis and Fertility. Wassarman PM, Litscher ES. Genes (Basel) 12 1266 (2021)
  3. Cryo-electron microscopy of cholinesterases, present and future. Leung MR, Zeev-Ben-Mordehai T. J Neurochem 158 1236-1243 (2021)
  4. Mechanistic interactions of uromodulin with the thick ascending limb: perspectives in physiology and hypertension. Boder P, Mary S, Mark PB, Leiper J, Dominiczak AF, Padmanabhan S, Rampoldi L, Delles C. J Hypertens 39 1490-1504 (2021)
  5. A Frame-by-Frame Glance at Membrane Fusion Mechanisms: From Viral Infections to Fertilization. Azimi FC, Dean TT, Minari K, Basso LGM, Vance TDR, Serrão VHB. Biomolecules 13 1130 (2023)
  6. Evolving Concepts in Uromodulin Biology, Physiology, and Its Role in Disease: a Tale of Two Forms. LaFavers KA, Micanovic R, Sabo AR, Maghak LA, El-Achkar TM. Hypertension 79 2409-2418 (2022)
  7. Fertilization of Ascidians: Gamete Interaction, Self/Nonself Recognition and Sperm Penetration of Egg Coat. Saito T, Sawada H. Front Cell Dev Biol 9 827214 (2021)
  8. Role of Uromodulin in Salt-Sensitive Hypertension. Mary S, Boder P, Padmanabhan S, McBride MW, Graham D, Delles C, Dominiczak AF. Hypertension 79 2419-2429 (2022)

Articles citing this publication (10)

  1. Cryo-EM structure of native human uromodulin, a zona pellucida module polymer. Stsiapanava A, Xu C, Brunati M, Zamora-Caballero S, Schaeffer C, Bokhove M, Han L, Hebert H, Carroni M, Yasumasu S, Rampoldi L, Wu B, Jovine L. EMBO J 39 e106807 (2020)
  2. Water Loading and Uromodulin Secretion in Healthy Individuals and Idiopathic Calcium Stone Formers. LaFavers KA, Gaddy AR, Micanovic R, Lingeman J, Williams JC, Coe FL, El-Achkar TM, Worcester E. Clin J Am Soc Nephrol 18 1059-1067 (2023)
  3. Sperm-binding regions on bovine egg zona pellucida glycoprotein ZP4 studied in a solid supported form on plastic plate. Dilimulati K, Orita M, Undram G, Yonezawa N. PLoS One 16 e0254234 (2021)
  4. N-Glycosylation Site in the Middle Region Is Involved in the Sperm-Binding Activity of Bovine Zona Pellucida Glycoproteins ZP3 and ZP4. Dilimulati K, Yulin Z, Imai FL, Yonezawa N. Biomolecules 13 1636 (2023)
  5. Egg envelope formation of medaka Oryzias latipes requires ZP proteins originating from both the liver and ovary. Yokokawa R, Watanabe K, Kanda S, Nishino Y, Yasumasu S, Sano K. J Biol Chem 299 104600 (2023)
  6. Structure of the decoy module of human glycoprotein 2 and uromodulin and its interaction with bacterial adhesin FimH. Stsiapanava A, Xu C, Nishio S, Han L, Yamakawa N, Carroni M, Tunyasuvunakool K, Jumper J, de Sanctis D, Wu B, Jovine L. Nat Struct Mol Biol 29 190-193 (2022)
  7. The kidney releases a nonpolymerizing form of uromodulin in the urine and circulation that retains the external hydrophobic patch domain. Micanovic R, LaFavers KA, Patidar KR, Ghabril MS, Doud EH, Mosley AL, Sabo AR, Khan S, El-Achkar TM. Am J Physiol Renal Physiol 322 F403-F418 (2022)
  8. Variation and Selection in the Putative Sperm-Binding Region of ZP3 in Muroid Rodents: A Comparison between Cricetids and Murines. Duarte MA, Fernandes CR, Heckel G, da Luz Mathias M, Bastos-Silveira C. Genes (Basel) 12 1450 (2021)
  9. ZP4 Is Present in Murine Zona Pellucida and Is Not Responsible for the Specific Gamete Interaction. Izquierdo-Rico MJ, Moros-Nicolás C, Pérez-Crespo M, Laguna-Barraza R, Gutiérrez-Adán A, Veyrunes F, Ballesta J, Laudet V, Chevret P, Avilés M. Front Cell Dev Biol 8 626679 (2020)
  10. Zona Pellucida like Domain Protein 1 (ZPLD1) Polymerization Is Regulated by Two Distinguished Hydrophobic Motifs. Knepper MI, Dernedde J. Int J Mol Sci 23 13894 (2022)


Related citations provided by authors (14)

  1. Characterization and separation of an inhibitor of viral hemagglutination present in urine.. TAMM I, HORSFALL FL Proc Soc Exp Biol Med 74 106-8 (1950)
  2. Etude chimique et ultrastructurale de la glycoproteine de Tamm et Horsfall ou uromucoide.. Delain E, Thiery JP, Coulard D, Joliviene A, Hartman L Biol. Cellulaire 39 31-42 (1980)
  3. Identification of human uromodulin as the Tamm-Horsfall urinary glycoprotein.. Pennica D, Kohr WJ, Kuang WJ, Glaister D, Aggarwal BB, Chen EY, Goeddel DV Science 236 83-8 (1987)
  4. The ZP domain is a conserved module for polymerization of extracellular proteins.. Jovine L, Qi H, Williams Z, Litscher E, Wassarman PM Nat Cell Biol 4 457-61 (2002)
  5. Tamm-Horsfall glycoprotein: biology and clinical relevance.. Serafini-Cessi F, Malagolini N, Cavallone D Am J Kidney Dis 42 658-76 (2003)
  6. A duplicated motif controls assembly of zona pellucida domain proteins.. Jovine L, Qi H, Williams Z, Litscher ES, Wassarman PM Proc Natl Acad Sci U S A 101 5922-7 (2004)
  7. Zona pellucida domain proteins.. Jovine L, Darie CC, Litscher ES, Wassarman PM Annu Rev Biochem 74 83-114 (2005)
  8. Analysis of uromodulin polymerization provides new insights into the mechanisms regulating ZP domain-mediated protein assembly.. Schaeffer C, Santambrogio S, Perucca S, Casari G, Rampoldi L Mol Biol Cell 20 589-99 (2009)
  9. Insights into egg coat assembly and egg-sperm interaction from the X-ray structure of full-length ZP3.. Han L, Monné M, Okumura H, Schwend T, Cherry AL, Flot D, Matsuda T, Jovine L Cell 143 404-15 (2010)
  10. The rediscovery of uromodulin (Tamm-Horsfall protein): from tubulointerstitial nephropathy to chronic kidney disease.. Rampoldi L, Scolari F, Amoroso A, Ghiggeri G, Devuyst O Kidney Int 80 338-47 (2011)
  11. The serine protease hepsin mediates urinary secretion and polymerisation of Zona Pellucida domain protein uromodulin.. Brunati M, Perucca S, Han L, Cattaneo A, Consolato F, Andolfo A, Schaeffer C, Olinger E, Peng J, Santambrogio S, Perrier R, Li S, Bokhove M, Bachi A, Hummler E, Devuyst O, Wu Q, Jovine L, Rampoldi L Elife 4 e08887 (2015)
  12. A structured interdomain linker directs self-polymerization of human uromodulin.. Bokhove M, Nishimura K, Brunati M, Han L, de Sanctis D, Rampoldi L, Jovine L Proc Natl Acad Sci U S A 113 1552-7 (2016)
  13. Structure of Zona Pellucida Module Proteins.. Bokhove M, Jovine L Curr Top Dev Biol 130 413-442 (2018)
  14. Cryo-EM structure of native human uromodulin, a zona pellucida module polymer.. Stsiapanava A, Xu C, Brunati M, Zamora-Caballero S, Schaeffer C, Han L, Carroni M, Yasumasu S, Rampoldi L, Wu B, Jovine L bioRxiv - (2020)

Quick links