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KIF14 binds tightly to microtubules and adopts a rigor-like conformation.

Arora K, Talje L, Asenjo AB, Andersen P, Atchia K, Joshi M, Sosa H, Allingham JS, Kwok BH
J Mol Biol 426 2997-3015 (2014)
Cited: 32 times
EuropePMC logo PMID: 24949858

Abstract

The mitotic kinesin motor protein KIF14 is essential for cytokinesis during cell division and has been implicated in cerebral development and a variety of human cancers. Here we show that the mouse KIF14 motor domain binds tightly to microtubules and does not display typical nucleotide-dependent changes in this affinity. It also has robust ATPase activity but very slow motility. A crystal structure of the ADP-bound form of the KIF14 motor domain reveals a dramatically opened ATP-binding pocket, as if ready to exchange its bound ADP for Mg·ATP. In this state, the central β-sheet is twisted ~10° beyond the maximal amount observed in other kinesins. This configuration has only been seen in the nucleotide-free states of myosins-known as the "rigor-like" state. Fitting of this atomic model to electron density maps from cryo-electron microscopy indicates a distinct binding configuration of the motor domain to microtubules. We postulate that these properties of KIF14 are well suited for stabilizing midbody microtubules during cytokinesis.

Reviews - 4ozq mentioned but not cited (2)

  1. Crystal structures of MBP fusion proteins. Waugh DS. Protein Sci 25 559-571 (2016)
  2. These motors were made for walking. Hunter B, Allingham JS. Protein Sci 29 1707-1723 (2020)

Articles - 4ozq mentioned but not cited (7)

  1. High-resolution structures of kinesin on microtubules provide a basis for nucleotide-gated force-generation. Shang Z, Zhou K, Xu C, Csencsits R, Cochran JC, Sindelar CV. Elife 3 e04686 (2014)
  2. Cryo-EM reveals the structural basis of microtubule depolymerization by kinesin-13s. Benoit MPMH, Asenjo AB, Sosa H. Nat Commun 9 1662 (2018)
  3. The divergent mitotic kinesin MKLP2 exhibits atypical structure and mechanochemistry. Atherton J, Yu IM, Cook A, Muretta JM, Joseph A, Major J, Sourigues Y, Clause J, Topf M, Rosenfeld SS, Houdusse A, Moores CA. Elife 6 e27793 (2017)
  4. Loss-of-function mutations in KIF14 cause severe microcephaly and kidney development defects in humans and zebrafish. Reilly ML, Stokman MF, Magry V, Jeanpierre C, Alves M, Paydar M, Hellinga J, Delous M, Pouly D, Failler M, Martinovic J, Loeuillet L, Leroy B, Tantau J, Roume J, Gregory-Evans CY, Shan X, Filges I, Allingham JS, Kwok BH, Saunier S, Giles RH, Benmerah A. Hum Mol Genet 28 778-795 (2019)
  5. Kinesin Motor Enzymology: Chemistry, Structure, and Physics of Nanoscale Molecular Machines. Cochran JC. Biophys Rev 7 269-299 (2015)
  6. Structural basis of mechano-chemical coupling by the mitotic kinesin KIF14. Benoit MPMH, Asenjo AB, Paydar M, Dhakal S, Kwok BH, Sosa H. Nat Commun 12 3637 (2021)
  7. Mechanochemical tuning of a kinesin motor essential for malaria parasite transmission. Liu T, Shilliday F, Cook AD, Zeeshan M, Brady D, Tewari R, Sutherland CJ, Roberts AJ, Moores CA. Nat Commun 13 6988 (2022)


Reviews citing this publication (7)

  1. Dissecting the Genetic and Etiological Causes of Primary Microcephaly. Jean F, Stuart A, Tarailo-Graovac M. Front Neurol 11 570830 (2020)
  2. Kinesin, 30 years later: Recent insights from structural studies. Wang W, Cao L, Wang C, Gigant B, Knossow M. Protein Sci 24 1047-1056 (2015)
  3. Molecular Genetics of Microcephaly Primary Hereditary: An Overview. Siskos N, Stylianopoulou E, Skavdis G, Grigoriou ME. Brain Sci 11 581 (2021)
  4. Inhibiting microcephaly genes as alternative to microtubule targeting agents to treat brain tumors. Iegiani G, Di Cunto F, Pallavicini G. Cell Death Dis 12 956 (2021)
  5. Emerging role of microtubule-associated proteins on cancer metastasis. Wattanathamsan O, Pongrakhananon V. Front Pharmacol 13 935493 (2022)
  6. Cytoskeletal and Cytoskeleton-Associated Proteins: Key Regulators of Cancer Stem Cell Properties. Li Y, Wang D, Ge H, Güngör C, Gong X, Chen Y. Pharmaceuticals (Basel) 15 1369 (2022)
  7. New insights into the mechanochemical coupling mechanism of kinesin-microtubule complexes from their high-resolution structures. Benoit MPMH, Hunter B, Allingham JS, Sosa H. Biochem Soc Trans 51 1505-1520 (2023)

Articles citing this publication (16)

  1. The structure of apo-kinesin bound to tubulin links the nucleotide cycle to movement. Cao L, Wang W, Jiang Q, Wang C, Knossow M, Gigant B. Nat Commun 5 5364 (2014)
  2. Mutations of KIF14 cause primary microcephaly by impairing cytokinesis. Moawia A, Shaheen R, Rasool S, Waseem SS, Ewida N, Budde B, Kawalia A, Motameny S, Khan K, Fatima A, Jameel M, Ullah F, Akram T, Ali Z, Abdullah U, Irshad S, Höhne W, Noegel AA, Al-Owain M, Hörtnagel K, Stöbe P, Baig SM, Nürnberg P, Alkuraya FS, Hahn A, Hussain MS. Ann Neurol 82 562-577 (2017)
  3. Biallelic variants in KIF14 cause intellectual disability with microcephaly. Makrythanasis P, Maroofian R, Stray-Pedersen A, Musaev D, Zaki MS, Mahmoud IG, Selim L, Elbadawy A, Jhangiani SN, Coban Akdemir ZH, Gambin T, Sorte HS, Heiberg A, McEvoy-Venneri J, James KN, Stanley V, Belandres D, Guipponi M, Santoni FA, Ahangari N, Tara F, Doosti M, Iwaszkiewicz J, Zoete V, Backe PH, Hamamy H, Gleeson JG, Lupski JR, Karimiani EG, Antonarakis SE. Eur J Hum Genet 26 330-339 (2018)
  4. Kinesin expands and stabilizes the GDP-microtubule lattice. Peet DR, Burroughs NJ, Cross RA. Nat Nanotechnol 13 386-391 (2018)
  5. KIF14 promotes cell proliferation via activation of Akt and is directly targeted by miR-200c in colorectal cancer. Wang ZZ, Yang J, Jiang BH, Di JB, Gao P, Peng L, Su XQ. Int J Oncol 53 1939-1952 (2018)
  6. Ternary complex of Kif2A-bound tandem tubulin heterodimers represents a kinesin-13-mediated microtubule depolymerization reaction intermediate. Trofimova D, Paydar M, Zara A, Talje L, Kwok BH, Allingham JS. Nat Commun 9 2628 (2018)
  7. Kinesin motility is driven by subdomain dynamics. Hwang W, Lang MJ, Karplus M. Elife 6 e28948 (2017)
  8. Neck linker docking is critical for Kinesin-1 force generation in cells but at a cost to motor speed and processivity. Budaitis BG, Jariwala S, Reinemann DN, Schimert KI, Scarabelli G, Grant BJ, Sept D, Lang MJ, Verhey KJ. Elife 8 e44146 (2019)
  9. The kinesin KIF14 is overexpressed in medulloblastoma and downregulation of KIF14 suppressed tumor proliferation and induced apoptosis. Li KK, Qi Y, Xia T, Chan AK, Zhang ZY, Aibaidula A, Zhang R, Zhou L, Yao Y, Ng HK. Lab Invest 97 946-961 (2017)
  10. Structural maintenance of chromosome (SMC) proteins link microtubule stability to genome integrity. Laflamme G, Tremblay-Boudreault T, Roy MA, Andersen P, Bonneil É, Atchia K, Thibault P, D'Amours D, Kwok BH. J Biol Chem 289 27418-27431 (2014)
  11. MiR-154-5p Suppresses Cell Invasion and Migration Through Inhibiting KIF14 in Nasopharyngeal Carcinoma. Chen J, Ma C, Zhang Y, Pei S, Du M, Zhang Y, Qian L, Wang J, Yin L, He X. Onco Targets Ther 13 2235-2246 (2020)
  12. The structural switch of nucleotide-free kinesin. Cao L, Cantos-Fernandes S, Gigant B. Sci Rep 7 42558 (2017)
  13. Kinesin-8-specific loop-2 controls the dual activities of the motor domain according to tubulin protofilament shape. Hunter B, Benoit MPMH, Asenjo AB, Doubleday C, Trofimova D, Frazer C, Shoukat I, Sosa H, Allingham JS. Nat Commun 13 4198 (2022)
  14. A neuropathy-associated kinesin KIF1A mutation hyper-stabilizes the motor-neck interaction during the ATPase cycle. Morikawa M, Jerath NU, Ogawa T, Morikawa M, Tanaka Y, Shy ME, Zuchner S, Hirokawa N. EMBO J 41 e108899 (2022)
  15. Global Gene Expression of Cultured Human Dermal Fibroblasts: Focus on Cell Cycle and Proliferation Status in Improving the Condition of Face Skin. Machaliński B, Rogińska D, Wilk A, Szumilas K, Prowans P, Paczkowska E, Szumilas P, Stecewicz I, Zawodny P, Ziętek M, Wiszniewska B. Int J Med Sci 18 1519-1531 (2021)
  16. Nucleotide-free structures of KIF20A illuminate atypical mechanochemistry in this kinesin-6. Ranaivoson FM, Crozet V, Benoit MPMH, Abdalla Mohammed Khalid A, Kikuti C, Sirkia H, El Marjou A, Miserey-Lenkei S, Asenjo AB, Sosa H, Schmidt CF, Rosenfeld SS, Houdusse A. Open Biol 13 230122 (2023)


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