doi: /nature19946 Proteins mediate the fundamental processes of life, and the beautiful
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1 PL,oSNAvT o o o ovo o Po-S H 1,2 *, So E Boyk 1,2,3 * & Dv Bk 1,2,3 T o o- q o 200- o, o w vooy o oy D ovo o xo q, y y o o Coo oooy v o o w o o w o-v y Ao o o vov oo o y o o; o ow o o w o o o o o k o oooy REVIEW o:101038/19946 Po o o, v wy w y o v o o o o 50 y Po- v o o ov v y o Fo y o o : o o y o ox o; v o o o (ooy o 1 ) o (oo 2 ); ovo o H o o (ATP y 3 ); oo o y o wok ( yo 4 ) No oy o k y o q o o w x ooy S q y -o o o, oo o o x oy o o oo ozo D v ooy o 100 y, - o o w o o o o o o y o o y -y T o o y o o v o k w o y y o voo I o w-o-o o vo o oo ow o ov ADP o ATP, v o o oy v o o o, w o o o o y w o I Rvw, w oo o o o o oy oy oo, o o o o o o v wo o oz o o o o kow o ow o wok y o o oy W o y o o o ovo o : o o w o o o y w q o o W ooo v o ovo o w ov ovvw o vy o o w -oo X-y yoy o o (NMR) o w o Ao o o vov oo o y o o o o o q voo 5 7, w vov y o vo ooy B o v xvy vw 8,9 y xo o vooy o, y w o I o y o o o o q o y y o o (F 1) T o q o o o o y q ( o o 200 o o 20 o ), o o o y x o o o o Evy, voo xo oy y o o q o o A voo o y o o, y o o o oy o q ;, y y o T ky o voo o ovo o Coqy, vooy o o oo o xoo y, y o y o Fo o o v v o o-q oo ( o-y) o I, o o o w o o o o o o o o oy O o o yo o o o ow y o o- q, oy oo y C A 13 Gv y o o o y o o, w o o o o o q, o o o q o o w T wo o:, y o y o o w y; o, o o q vy o o ovy I Rvw, w y o y o o o o ovo o T o o o x o vo Ro o oooy 14 ; o ovo o ow w Co o o o oy o v oo o o o Rvw, o o v wo o T o: ovo o ooy xv, y vy o o 1 D o Boy, Uvy o Wo, S, Wo 98195, USA 2 I o Po D, Uvy o Wo, S, Wo 98195, USA 3 How H M I, Uvy o Wo, S, Wo 98195, USA *T o o qy o wok P : D o Bo, So Uvy, So, Co 94305, USA 320 NATURE SEPTEMBER M
2 016MPL,oSN Nv o D voo D ovo o F 1 Mo o ovo o, A o o q Evoo oy y o o o o q (), o voo y o v o (), w oo o o v o xo oy D voo o o o q o v o, w ovo o xo wo, S o, x-ko ovo o o ozo o w y o o o I o, q x ko kow; x ko o, q kow x; ovo o, kow, Ex o y o x-q o- o o T o ow-y o Mo Co jo, w o o o y o (k o) o x x; y y oo--q vo () I ovo o, q o w o ov o o x zo, B, ovo o () o o o o (CASP)11 T0806, w o q y o y o o kow, ovoo-v o o 27 T y (Po D Bk o o 5CJA) ow o oo () T y o o o w w o w v o y - o y o o o x ow y wok w, o w w o vo o o Ro@o oj T o v y o DNA B o o o x, o o- q o o o x To o o o E o, y o o- q Mo o DNA y v ov y 10 y, y o o yz o ovo o o oo xy Py o T v o o o o o yoo o o, wy o ov To z z o vy o o w, o xz v W o, o k oy wo y vo o ov Po o w ov o o o o o o -o yo o o o, ow y o o w w vo o 18 T k o o o oow o oo: α- β- oy, w o oy o o oy ko o yo o, wy o-o o k o jw zz o o y k o Io o o- w o ko o o o o y o o: yo o o α- oo vo ko o vo o Fo x, o o o w oy ow o ko, w y, w k, o ko oo w oy T o o o y o o o o o w o w ov T oo o y o v W o vo o o k, o, o o yo o, ovo oo o ko - o P o y o q o o v ko - ooo o y q w vy ow y D o o ko - S o Sq kow, kow Fx-ko Sq kow, kow D ovo Sq kow, kow I: Kow o- q Kow ko A o Bko G y o v q S- Ro o v o Bko No S- Ro o o Bko Sq S- Ro o o O: P D q D ko q CASP11 T0806 Ey Po Cy 15 SEPTEMBER 2016 VOL 537 NATURE 321 AvREVIEW 2INSIGHT
3 INSIGHT REVIEW F 2 D αβ o, S v ko o β---α-x o y, D ovo αβ o w -oo NMR o X-y vy o w o28,36,37, To7, Fox o o vy z, Ro 2 2 o, IF3-k o, P-oo 2 2 o, Ro 3 1 o, L, o ox w o o 38 (F 1) I -, oo ozo o y o - ooo (kow o) o ow-y, oy k o o19 22 I o- q kow v, o o o ( o o o o- q), o- v y x ov o o B q kow, o o ( q o o ), o o- o Bko o o ozo o y k v o o q ow o o o I o, oo ozo o q-nwo zo o - k o o yo o o Po- o I o o o o o: ow y o x o- q o oo o o vooy o B o- q x, - oo ozo ov oy vo o ko o o w o q23 A v o o vy o o w o q oy vo o y o o w o q o w y ooo I o o wo ooo o kow o o T z o ko ooo : o y ow o y v, vy o Howv, y x o o oo, o-voo- o24,25, -o o v- y (F 1) I,, o o ox o 26,27 (F 1) D ovo o F 3 D o w yy, T oo o, D ovo o w -oo X-y vy o w o, D ovo α- oo41, A TIM w o-o yy Pk (w) oo (k ) ow42, T o w vy o w v o yo ooo ov 43 v A N S o, L P M NAT U R E S E P T E M B E R Uk -o x-ko o, ( ovo) o o, o q x o ko kow (F 1) Gv, ow o w vy ko o? B oy ooo o ko ooo oo q w o- o k yo o w yo-o oo o, o y w o (o 10,000) v ooo T ko y o 28,29 o y qo o y oy y30 35 Fo ko ooo, oo qozo o o y ow-y q o A o -o o o o w
4 REVIEW INSIGHT P (ϕ1) Oo yy (ϕ0) Oo (+/ ) S w (ω0) Z o (Z0) C2 α-hx (ω1) C3 C4 C5 C6 C7 C2 C3 C3 F 4 D ovo ko o, P oy, T ovo o y v: α3d ( 48) () RH4 ( 30) (), - o o, Fo ovo : o o- x53 (), Z2+ o o (kow Rok)34, S- y 33: - o-x () w -x (), Hoo-oo - 31,33,51,52, Hoo-oo ovo o o-y w yo-o wok- y63; o wok ow x o-o C -o y yy oo: o x, C2 oo C3 oo ow-y o q o o oy k D ovo y xy z oy -o o o q oy ov o (F 1) Oy o ko ooy To k o o q- ko oo, y o oo o o ko o o o, o o o w o oy q x wo ow-y Po ow o q vo o q- o o ko oy O o o o ovy o oy q o o o ko k yo o w α- o β- o o o o w ov xo oo T o y o oy o v oooy36 Ao o o o xy o oy, w o oo o α- β- vo k oo37 So y o o v v q- o, oo w k o y oo o ooo o o α- β-36,37 Ev w o, o o ko To w o o o o o o o o o o o, ovo o- wok o o w kk α- β- oo By o, o y o o o, o-o o o o o o o S o y o o y o o (D voo, w oy o oz y o o yo 8 k o, w oo o o- oo o o 99999%) I αβ o A w o αβ o v q- 36,37 (F 2) T o o o v F, ov oooy 29 o w ko o y, k o o o α- β-, w o o oo So, o ko o w o o Mo Co o (F 2) T, oo o ozo o y ow-y o- q o ko Fo, y o ko xo q ozo o o v q w vy ow y L, q ov o oo o o xy T o w o z ko ow F 2 Sy o w o w, o w o E o T o w o o xy w o o o o o28,36 38 (F 2) v A N S o, L P M S E P T E M B E R VO L NAT U R E 3 2 3
5 INSIGHT REVIEW F 5 D - o, C2, C3, C4 C5 y oo-oo ( 78 J F G U, o oo), Two-o xo 81, S-, A o-oo o () o-oo oo79 (), Two-oo o80; wo y oo oo yow, A o-oo y oo w ovo ( ) o 82, Two-oo o- o83; wo oo o oo yow R o T o o o ovo o w ko o o o w yy w z o (F 3) I yy z o q vy w kow q oo o y o o (F 3) T o o yy y o o o w jxo w, α- oo41 (F 3) TIM 42 (F 3) I TIM, ko, o w oy o o β-, k o-o yy o wo α- α β α β o 42 Bo o- o- o v o y o y o E o, oow y x zo o o H-oo X-y yoy o w o o o o o T α- v q (F 3) y o o o o, w y o o oy y o o o z43 T w o xoy ; v o o oy y yoo oo o o 6 M (D Bk, o oo) By o, o o o o o x-o o y o o w o o o v 44 oo o q o o Co oo o v o o o w ko 45, o o o oy yy v o z o46 Hyo-o wok T w v o o ovo o oo o y o o oo y o o o, w o B v y w o yoo k o o o ov oo ov y I o o o x o DNA, w y o yo o o oo o -y o, yo v A N S o, L P M NAT U R E S E P T E M B E R P T o qo oy o o ko ov o oo ov o Eqo vo y F Ck o o z o α- o oo w v y,, v oo w47 (F 4) T y q- o, y - oo, o o w oo o y My v wy30,31,33,34,48 52 (F 4), o o o53, - 31, o o34, 54 α- w yoy vy55 T oo o ko o w oo - ozo o, o v 33; k y ovo o, y o xy, o 7 M yoo 95 C
6 016MPL,oSN15 SEPTEMBER 2016 VOL 537 NATURE 325 Av * * * * * F 6 D y ovo o,, D ok o w wo () o () k (yow ), Cy w ovy k N C A k o o o x o -o -o o o o y o o y vy o 62 A w o o o yo-o oo o o o yo o I y, o o o w o-v y xv wok o yo o w o o oo o 63 T o - oo o w y y y o yo-o wok, oo o Wo Ck - DNA 64 Io o ko o o o wok o yo o q o o o o ko I o DNA oooy 61, o Wo Ck yo o o w o 65,66 ; o o o o o o o o yo-o wok o o y T o w o T v Rvw, o o w w 3 y, o o o o o o v T kow w vy o xoy o o w o-v y (T -oo o o o Rvw, y NMR, X-y yoy o o ooy, o w o) T o o w o o o o o o ovo ko o o y v o oo o- o, w o o y o o v o o y o o S o v y zy v y o voo 67 73, o o o o o o o v o 74 -o o oo o vvo oo T o w o o o, y oo-oo ( 78 J F G U, o oo), 79,80, o 79 o woo 81 (F 5) Po o v o o- o wo-oo w oo yy o , vy T yy o v o o o v o, vo o o w o k o o vy o T o o B o v o oo ovo o o, REVIEW 2INSIGHT o x o o o o o y x o o -o o o v o T o o o o ovo o o o yo o ov w o y oo w o A x o o y, w o y ok y k o N C 84 I, xo o oooy o -o -o w o (F 6) T o, xy o NMR X-y yoy, o o o, oy 15 50, o xy o o Iov o o ovo A o o ovo o oy o o o o o w o E o T o q o o oy oo o oo (oyy) xy -oo o o oo o wy vy o o o o Ioy oyy oy o o yoo o I o o w q ov y o y o o (o x, x o o o o o o w o w o), o x v o vo v o v oo oooy A o o yz DNA x zo o o o, o o y o o y w o o I o y o o o Rvw T o wok o o o w o o y 84, o w v o w o oo w o o o; v ooo o T w o yz y ow o o x oy o oxy o o E o o o o ox o ooy T α- y wok o yo o oy o o 90%, o 60% o w oo oozo 63 B y o o o o o yo o, o-k w yo o o o vo O α- 43, 90% w o
7 PL,oSNAvREVIEW INSIGHT 64% w oo Ao o oo - X-y w o w o 84 H, q o oy vo w ov v Oook A o o w y o o o v w o y o o o o- o o o w vy o ; o y y o zy v oo oo 85 Nv o o y, q o o o o T vy y o ovo o o k o o o o w o T x o o wo T y o o o ovo o oy o o y, oo o o w vy oo y Po o o o y v yoo o o o o o o z o o o o o v Rvw, v o zy v o oy o o o o v R v, w o oo o o ovo o, w q o Ny o o ov o x o oy, oy, o y w owy ov o y x To v, w o v w o o o o k o o o oo o o, w q o o w, y (By o, ovo F 2 6 v, y (F 1)) T o o z-o o wo v o o ow o v oxy 34 Ovo y x o S wo oo v oo o o o So A o Io A I o w o o o y x, o ow v o y w o o ov o j o ooy o o o o ooy Rv 12 A; 20 Jy F, S How ooy y k o N 413, (2001) 2 Ro, D M, R, S G F & Kok, B K T o o G-o-o o N 459, (2009) 3 Yo, M, Myk, E & Ho, T ATP y vo oy o N Rv Mo C Bo 2, (2001) 4 S, J A T yo w o- o N Rv Mo C Bo 2, (2001) 5 Doy, M J & Ao, F H D voo: w oz o C O Boo 20, (2009) 6 Ao, F H T o ovo: w zy y voo Q Rv Boy 48, (2015) 7 Go, M & Twk, D S D zy voo: yo ow C O S Bo 22, (2012) 8 Koy, G A, Sk, J, K, C A & Fo, C A Po o ovo o o ooo o T Boo 32, (2014) 9 R, L Po :,, Booy 104, (2015) 10 K, A D & Szok, J W Fo o o o-q y N 410, (2001) 11 F, M A, MKy, K L, By, L H, Vo, S R & H, M H D ovo o o y o q o E o ow PLoS ONE 6, (2011) 12 My, G S, G, J B & H, M H D ovo o w - o y y J Mo Bo 428, (2016) 13 E, C J, Go, R F & A, C B T oo o y o : w o y Co S H S Q Bo 28, (1963) 14 Lv-Fy, A ROSETTA3: oj-o ow o o o oo Mo Ezyo 487, (2011) 15 Woo, C W CCB: v w- oo o, o-o o Boo 30, (2014) 16 No, C & K, A E M o CLEVER CLASSY Mo Ezyo 523, (2013) 17 Sk, J, Po, M B, Koy, G A, Tyo, M S & Fo, C A Po WISDOM: wok o o ovo o oo J V Ex 77, (2013) 18 F, P J & Ro, G D Do ko o o o o yo o? Po S 14, (2005) 19 Po, J W & R, F M Ty o o: o k o o ow q o J Mo Bo 193, (1987) 20 Dy, B I & Myo, S L Po oo Po S 5, (1996) 21 Dy, B I & Myo, S L D ovo o : y o q o S 278, (1997) 22 K, B & Bk, D Nv o q o o o o Po N A S USA 97, (2000) 23 So, K T, Koo, C, H, E & Bk, D Ay o o y o w o q By o o J Mo Bo 268, (1997) 24 Bk, S, Ky, H, Co, J G, L, S-I & L, C J L v o o o o Po 79, (2011) 25 Ky, H, Ovkov, S & Bk, D A y o ovoo o o q- - Po N A S USA 110, (2013) 26 Ovkov, S, Ky, H & Bk, D Ro o o o o o vooy oo L 3, (2014) 27 Ovkov, S L- o o voy ov o vooy oo L 4, (2015) 28 K, B D o ov o o o w o-v y S 302, (2003) D To7, o o o w o o ov 29 H, P-S RoRo: z wok o x ko o PLoS ONE 6, (2011) 30 Hy, P B, P, J J, To, B, A, T & K, P S H-oo o w ko o S 282, (1998) D RH4, o o x-ko o qo 31 Too, A R Coo o w-o α- S 346, (2014) 32 Goy, G & DGo, W F Po y v z o o oy J Mo Bo 405, (2011) 33 H, P-S H oy y o y S 346, (2014) 34 Jo, N H D ovo o Z 2+ -o o-x S 346, (2014) P o o ovo (kow Rok) o Z 2+ Co 2+, o C 2+, o 35 R, L & DGo, W F Czo o o o S 241, (1988) 36 L, Y-R Coo ov ov z ovo o Po N A S USA 112, E5478 E5485 (2015) 37 Ko, N P o o N 491, (2012) E q-, w o v αβ ooo 38 K, I C P y o ox ooo o ovo ok L 4, (2015) 39 Rä, S, W, U, Mo, J, Akk, M & Aé, I Coo o - o w oy Po N A S USA 111, (2014) 40 Pk, K Coo o -o v y oo o N S Mo Bo 22, (2015) 41 Doy, L Ro o α- o w o N 528, (2015) 42 H, P-S D ovo o o-o y TIM- o w o-v y N C Bo 12, (2016) T y v o TIM 43 B, T J Exo o v o oo o N 528, (2015) 44 Jo, T M D o y o y voo S 352, (2016) 45 My, G S I q vy w x ko o : o o o yoo o S 20, (2012) 46 Co, B E Poo o o o-o v N 507, (2014) 326 NATURE SEPTEMBER M
8 016MPL,oSN47 Ck, F H C T k o α-: o-o A Cy 6, (1953) 48 W, S T, C, H, Byo, J W, Ro, H & DGo, W F Soo y o ovo -x o Po N A S USA 96, (1999) 49 F, J M A o ovo o-o oo o o o y ooy ACS Sy Bo 1, (2012) 50 Z, N R A ovo x w N C Bo 7, (2011) 51 E, D T, y, yzo o - Po 1, (1986) 52 K, A E, Mkv, V N, To, B & K, P S S- k o o o o o o Po N A S USA 98, (2001) 53 Goy, G Coo o v-k o o o o S 332, (2011) D o o o -w o o 54 F, J M S- o o-o o S 340, (2013) 55 Bo, A J, Too, A R, Dwo, W M, By, R L & Wooo, D N I yoy vy o oy ovo o wok N C ://xoo/101038/2555 (2016) 56 Goy, G, Rk, A W & K, A E D o o-o y v v ZIP- N 458, (2009) 57 Rk, A W, G, R A & K, A E A y o-o o ov o o o o J A C So 132, (2010) 58 Loo, N & Aoo, X A o o ovo oo o o o: yo, y w J S Bo 185, (2014) 59 Gš, H D o - oy o o o-o N C Bo 9, (2013) 60 Gš, H & J, R D ovo o ooo o o-o o J P S 17, (2011) 61 S, G & K, A E Po y v oy C O S Bo 21, (2011) 62 S, P B & K, B A oo o o o yo o Po S 22, (2013) 63 Boyk, S E D ovo o o oo-oo w o yo-o wok- y S 352, (2016) D o w xv yo-o wok o y oo o DNA 64 S, N C DNA wo N 421, (2003) 65 Lko, V & Dz, H T o DNA oooy C O Boo 24, (2013) 66 Z, F, Nv, J, L, Y & Y, H S DNA oooy: o v J A C So 136, (2014) 67 Hv, D D o o y A Rv Bo 82, (2013) 68 K, H, Bo, R & Hv, D D ovo zy y oo C O C Bo 17, (2013) REVIEW 2INSIGHT 69 K, G, Ç-Öçü, N, Mo, R, Bk, D & Hok, K N Coo zy Aw C I E E 52, (2013) 70 R, F, Lv-Fy, A, K, S D, Bj, S & Bk, D D ovo zy Ro3 PLoS ONE 6, (2011) 71 Bk, D A x o o oo zy Po S 19, (2010) 72 K, G, Rö, D, Bk, D & Hok, K N Evo k o zy Po S 19, (2010) 73 Go, X, Wky, B I & Hv, D F Kov oo yz y S--o zy J A C So 138, (2016) 74 Koy, M T A ooy - o ov vvo oo o z o o o PLoS Po 12, (2016) 75 T, C E Coo o - o w y vy N 501, (2013) 76 G, R Bo o o o o-o- oo N C Bo 10, (2014) 77 F, J A y o o o oo kyo L 4, (2015) 78 Mo, Y, H, P-S, H, F-C, H, S-J & Myo, S L Coo x vo o y o oo Po N A S USA 112, (2015) 79 K, N P Coo o - o o w o v y S 336, (2012) 80 K, N P A o o- -oo o o N 510, (2014) 81 Go, S, Do, F, Go, T & Bk, D D o o wo-o y y oov o-o S 348, (2015) 82 H, Y D o y 60- o oo N 535, (2016) 83 B, J B A o o- wo-oo o o ox S 353, (2016) 84 Bwj, G, M, V K, B, C D & Bk, D A ovo o y o N ://xoo/101038/ (2016) T o y o oo o - -o 85 G, L Evoo o o-o o o v o N C Bo 9, (2013) Akow W k o Bk ooy I o Po D Uvy o Wo, w RoCoo oy W ooz o o wo wok w w o kow o o o T o o y How H M I (HHMI ) Ao Ioo R o oo v wwwo/ T o o o R wo o o o o vo o oo/2qvj Coo o o DB (k@w) 15 SEPTEMBER 2016 VOL 537 NATURE 327 Av
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