Hướng tới việc lắp ráp một divisome tối thiểu

Springer Science and Business Media LLC - Tập 8 - Trang 237-247 - 2014
Zohreh Nourian1, Andrew Scott1, Christophe Danelon1
1Department of Bionanoscience, Kavli Institute of Nanoscience, Delft University of Technology, Delft, the Netherlands

Tóm tắt

Việc xây dựng một tế bào tối thiểu không thể giảm thiểu, có đầy đủ các thuộc tính thiết yếu của một hệ thống sống là một trong những thách thức lớn nhất mà sinh học tổng hợp phải đối mặt. Một nhiệm vụ phổ biến mà mọi hệ thống sống đều thực hiện là phân chia vỏ tế bào. Do đó, việc lắp ráp một công cụ phân tử cơ bản, mặc dù đầy đủ, hỗ trợ cho việc phân chia ngăn, là một bước quan trọng hướng tới việc hiện thực hóa các tế bào nhân tạo tự sinh sản. Nhìn lại bản chất phân tử của các hệ thống phân chia tế bào có thể là tổ tiên, có thể là thô sơ hơn, có thể giúp xác định một divisome tối thiểu. Dựa trên một con đường tiến hóa khả thi của các cơ chế phân chia từ các túi lipid đơn giản dẫn đến sự sống hiện đại, chúng tôi xác định hai cách tiếp cận để tái tạo phân chia trong các tế bào nguyên thủy: con đường protein biến dạng màng và con đường tổng hợp lipid. Sau khi xác định các protein và cơ chế hoạt động có thể tham gia vào việc thay đổi hình dạng màng, chúng tôi thảo luận về cách mà các protein này có thể được tích hợp vào khung xây dựng của một tế bào tối thiểu có thể lập trình, dựa vào sự biểu hiện gen bên trong các liposome. Hệ thống tổng hợp protein sử dụng các yếu tố tái tổ hợp (PURE), một hệ thống biểu hiện gen tối thiểu đã được tái tạo, có thể coi là nền tảng tổng hợp đa dạng nhất. Là bước đầu tiên hướng tới việc tổng hợp de novo một divisome, chúng tôi đã chỉ ra rằng protein miền N-BAR được sản xuất từ gen của nó có thể lắp ráp lên bề mặt bên ngoài của các liposome và định hình màng thành các cấu trúc ống. Cuối cùng, chúng tôi thảo luận về những thách thức còn lại cho việc xây dựng một tế bào tối thiểu tự sinh sản, đặc biệt là việc ghép nối máy phân chia với quá trình mở rộng thể tích và sao chép genome.

Từ khóa


Tài liệu tham khảo

Adams DW, Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7(9):642–653 Ahlquist P (2006) Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat Rev Microbiol 4(5):371–382 Allan EJ, Hoischen C, Gumpert J (2009) Bacterial L-forms. Adv Appl Microbiol 68:1–39 Almendro-Vedia VG, Monroy F, Cao FJ (2013) Mechanics of constriction during cell division: a variational approach. PLoS One 8(8):e69750 Bernander R, Ettema TJ (2010) FtsZ-less cell division in archaea and bacteria. Curr Opin Microbiol 13(6):747–752 Bhatia VK, Madsen KL, Bolinger PY, Kunding A, Hedegård P, Gether U, Stamou D (2009) Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J 28(21):3303–3314 Briers Y, Walde P, Schuppler M, Loessner MJ (2012) How did bacterial ancestors reproduce? Lessons from L-form cells and giant lipid vesicles: multiplication similarities between lipid vesicles and L-form bacteria. Bioessays 34(12):1078–1084 Cabre EJ, Sanchez-Gorostiaga A, Carrara P, Ropero N, Casanova M, Palacios P, Stano P, Jimenez M, Rivas G, Vicente M (2013) Bacterial division proteins FtsZ and ZipA induce vesicle shrinkage and cell membrane invagination. J Biol Chem 288(37):26625–26634 Caschera F, Noireaux V (2014) Synthesis of 2.3 mg/ml of protein with an all Escherichia coli cell-free transcription-translation system. Biochimie 99:162–168 Caspi Y, Dekker C (2014) Divided we stand: splitting synthetic cells for their proliferation. Syst Synth Biol Dannhauser PN, Ungewickell EJ (2012) Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat Cell Biol 14(6):634–639 Darwin CC (1859) The origins of the species by means of natural selection or the preservation of favoured races in the struggle for life. John Murray, London Diaz A, Ahlquist P (2012) Role of host reticulon proteins in rearranging membranes for positive-strand RNA virus replication. Curr Opin Microbiol 15(4):519–524 Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74(4):504–528 Forster AC, Church GM (2006) Towards synthesis of a minimal cell. Mol Syst Biol 2:45 Frost A, Perera R, Roux A, Spasov K, Destaing O, Egelman EH, De Camilli P, Unger VM (2008) Structural basis of membrane invagination by F-BAR domains. Cell 132(5):807–817 Gibson DG, Glass JI, Lartigue C, Noskov VN, Chuang RY, Algire MA, Benders GA, Montague MG, Ma L, Moodie MM, Merryman C, Vashee S, Krishnakumar R, Assad-Garcia N, Andrews-Pfannkoch C, Denisova EA, Young L, Qi ZQ, Segall-Shapiro TH, Calvey CH, Parmar PP, Hutchison CA 3rd, Smith HO, Venter JC (2010) Creation of a bacterial cell controlled by a chemically synthesized genome. Science 329(5987):52–56 Hanczyc MM, Szostak JW (2004) Replicating vesicles as models of primitive cell growth and division. Curr Opin Chem Biol 8(6):660–664 Hanczyc MM, Fujikawa SM, Szostak JW (2003) Experimental models of primitive cellular compartments: encapsulation, growth, and division. Science 302(5645):618–622 Hill NS, Buske PJ, Shi Y, Levin PA (2013) A moonlighting enzyme links Escherichia coli cell size with central metabolism. PLoS Genet 9(7):e1003663 Hu Z, Gogol EP, Lutkenhaus J (2002) Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc Natl Acad Sci USA 99(10):6761–6766 Jewett MC, Forster AC (2010) Update on designing and building minimal cells. Curr Opin Biotechnol 21(5):697–703 Jimenez M, Martos A, Vicente M, Rivas G (2011) Reconstitution and organization of Escherichia coli proto-ring elements (FtsZ and FtsA) inside giant unilamellar vesicles obtained from bacterial inner membranes. J Biol Chem 286(13):11236–11241 Koonin EV, Mulkidjanian AY (2013) Evolution of cell division: from shear mechanics to complex molecular machineries. Cell 152(5):942–944 Kurihara K, Tamura M, Shohda KI, Toyota T, Suzuki K, Sugawara T (2011) Self-reproduction of supramolecular giant vesicles combined with the amplification of encapsulated DNA. Nat Chem 3(10):775–781 Kuruma Y, Stano P, Ueda T, Luisi PL (2009) A synthetic biology approach to the construction of membrane proteins in semi-synthetic minimal cells. Biochim Biophys Acta Biomembr 1788(2):567–574 Kuruma Y, Suzuki T, Ono S, Yoshida M, Ueda T (2012) Functional analysis of membranous Fo-a subunit of F1Fo-ATP synthase by in vitro protein synthesis. Biochem J 442(3):631–638 Leaver M, Dominguez-Cuevas P, Coxhead JM, Daniel RA, Errington J (2009) Life without a wall or division machine in Bacillus subtilis. Nature 457(7231):849–853 Lindas AC, Karlsson EA, Lindgren MT, Ettema TJ, Bernander RA (2008) A unique cell division machinery in the archaea. Proc Natl Acad Sci USA 105:18942–18946 Liu YJ, Hansen GP, Venancio-Marques A, Baigl D (2013) Cell-free preparation of functional and triggerable giant proteoliposomes. ChemBioChem 14(17):2243–2247 Loakes D, Holliger P (2009) Darwinian chemistry: towards the synthesis of a simple cell. Mol BioSyst 5(7):686–694 Low HH, Löwe J (2006) A bacterial dynamin-like protein. Nature 444(7120):766–769 Low HH, Sachse C, Amos LA, Löwe J (2009) Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell 139(7):1342–1352 Luisi PL (2002) Toward the engineering of minimal living cells. Anat Rec 268(3):208–214 Luisi PL, Ferri F, Stano P (2006) Approaches to semi-synthetic minimal cells: a review. Naturwissenschaften 93(1):1–13 Macia J, Solé RV (2007) Synthetic turing protocells: vesicle self-reproduction through symmetry-breaking instabilities. Philos Trans R Soc Lond B Biol Sci 362(1486):1821–1829 Maeda YT, Nakadai T, Shin J, Uryu K, Noireaux V, Libchaber A (2012) Assembly of MreB filaments on liposome membranes: a synthetic biology approach. ACS Synth Biol 1(2):53–59 Makarova KS, Yutin N, Bell SD, Koonin EV (2010) Evolution of diverse cell division and vesicle formation systems in archaea. Nat Rev Microbiol 8(10):731–741 Mansy SS, Szostak JW (2009) Reconstructing the emergence of cellular life through the synthesis of model protocells. Cold Spring Harb Symp Quant Biol 74:47–54 Mattila PK, Pykäläinen A, Saarikangas J, Paavilainen VO, Vihinen H, Jokitalo E, Lappalainen P (2007) Missing-in-metastasis and IRSp53 deform PI(4,5)P2-rich membranes by an inverse BAR domain-like mechanism. J Cell Biol 176(7):953–964 McMahon HT, Gallop JL (2005) Membrane curvature and mechanisms of dynamic cell membrane remodeling. Nature 438:590–596 Mercier R, Kawai Y, Errington J (2013) Excess membrane synthesis drives a primitive mode of cell proliferation. Cell 152(5):997–1007 Mim C, Unger VM (2012) Membrane curvature and its generation by BAR proteins. Trends Biochem Sci 37:526–533 Morowitz HJ, Heinz B, Deamer DW (1988) The chemical logic of a minimum protocell. Orig Life Evol Biosph 18(3):281–287 Moya A, Gil R, Latorre A, Peretó J, Pilar Garcillán-Barcia M, de la Cruz F (2009) Toward minimal bacterial cells: evolution vs. design. FEMS Microbiol Rev 33(1):225–235 Murtas G (2009) Artificial assembly of a minimal cell. Mol BioSyst 5(11):1292–1297 Murtas G (2010) Internal lipid synthesis and vesicle growth as a step toward self-reproduction of the minimal cell. Syst Synth Biol 4(2):85–93 Murtas G (2013) Early self-reproduction, the emergence of division mechanisms in protocells. Mol BioSyst 9(2):195–204 Noireaux V, Libchaber A (2004) A vesicle bioreactor as a step toward an artificial cell assembly. Proc Natl Acad Sci USA 101(51):17669–17674 Noireaux V, Bar-Ziv R, Godefroy J, Salman H, Libchaber A (2005) Toward an artificial cell based on gene expression in vesicles. Phys Biol 2(3):P1–P8 Noireaux V, Maeda YT, Libchaber A (2011) Development of an artificial cell, from self-organization to computation and self-reproduction. Proc Natl Acad Sci USA 108(9):3473–3480 Nomura SM, Tsumoto K, Hamada T, Akiyoshi K, Nakatani Y, Yoshikawa K (2003) Gene expression within cell-sized lipid vesicles. ChemBioChem 4(11):1172–1175 Nourian Z, Danelon C (2013) Linking genotype and phenotype in protein synthesizing liposomes with external supply of resources. ACS Synth Biol 2(4):186–193 Nourian Z, Roelofsen W, Danelon C (2012) Triggered gene expression in fed-vesicle microreactors with a multifunctional membrane. Angew Chem Int Ed 51(13):3114–3118 Osawa M, Erickson HP (2013) Liposome division by a simple bacterial division machinery. Proc Natl Acad Sci USA 110(27):11000–11004 Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320(5877):792–794 Osawa M, Anderson DE, Erickson HP (2009) Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J 28(22):3476–3484 Peter BJ, Kent HM, Mills IG, Vallis Y, Butler PJ, Evans PR, McMahon HT (2004) BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303(5657):495–499 Peterlin P, Arrigler V, Kogej K, Svetina S, Walde P (2009) Growth and shape transformations of giant phospholipid vesicles upon interaction with an aqueous oleic acid suspension. Chem Phys Lipids 159(2):67–76 Saarikangas J, Zhao H, Pykäläinen A, Laurinmäki P, Mattila PK, Kinnunen PK, Butcher SJ, Lappalainen P (2009) Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr Biol 19(2):95–107 Saksena S, Wahlman J, Teis D, Johnson AE, Emr SD (2009) Functional reconstitution of ESCRT-III assembly and disassembly. Cell 136:97–109 Sakuma Y, Imai M (2011) Model system of self-reproducing vesicles. Phys Rev Lett 107(19):198101 Samson RY, Bell SD (2009) Ancient ESCRTs and the evolution of binary fission. Trends Microbiol 17(11):507–513 Samson RY, Obita T, Freund SM, Williams RL, Bell SD (2008) A role for the ESCRT system in cell division in archaea. Science 322(5908):1710–1713 Samson RY, Obita T, Hodgson B, Shaw MK, Chong PLG, Williams RL, Bell SD (2011) Molecular and structural basis of ESCRT-III recruitment to membranes during archaeal cell division. Mol Cell 41(2):186–196 Schmidli PK, Schurtenberger P, Luisi PL (1991) Liposome-mediated enzymatic synthesis of phosphatidylcholine as an approach to self-replicating liposomes. J Am Chem Soc 113(21):8127–8130 Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671–675 Schwille P (2011) Bottom-up synthetic biology: engineering in a tinkerer’s world. Science 333(6047):1252–1254 Shih YL, Huang KF, Lai HM, Liao JH, Lee CS, Chang CM, Mak HM, Hsieh CW, Lin CC (2011) The N-terminal amphipathic helix of the topological specificity factor MinE is associated with shaping membrane curvature. PLoS One 6(6):e21425 Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, Nishikawa K, Ueda T (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19(8):751–755 Shimizu Y, Kanamori T, Ueda T (2005) Protein synthesis by pure translation systems. Methods 36(3):299–304 Shimizu Y, Kuruma Y, Kanamori T, Ueda T (2014) The PURE system for protein production. Methods Mol Biol 1118:275–284 Shin J, Noireaux V (2010) Efficient cell-free expression with the endogenous E. Coli RNA polymerase and sigma factor 70. J Biol Eng 4:8 Sorre B, Callan-Jones A, Manzi J, Goud B, Prost J, Bassereau P, Roux A (2012) Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc Natl Acad Sci USA 109(1):173–178 Stahelin RV, Long F, Peter BJ, Murray D, De Camilli P, McMahon HT, Cho W (2003) Contrasting membrane interaction mechanisms of AP180 N-terminal homology (ANTH) and epsin N-terminal homology (ENTH) domains. J Biol Chem 278(31):28993–28999 Stano P, Luisi PL (2010) Achievements and open questions in the self-reproduction of vesicles and synthetic minimal cells. Chem Commun 46(21):3639–3653 Suefuji K, Valluzzi R, RayChaudhuri D (2002) Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE. Proc Natl Acad Sci USA 99(26):16776–16781 Svetina S (2009) Vesicle budding and the origin of cellular life. ChemPhysChem 10(16):2769–2776 Szostak JW, Bartel DP, Luisi PL (2001) Synthesizing life. Nature 409(6818):387–390 Takakura K, Toyota T, Sugawara T (2003) A novel system of self-reproducing giant vesicles. J Am Chem Soc 125(27):8134–8140 Takamura H, Koyama Y, Matsuzaki S, Yamada K, Hattori T, Miyata S, Takemoto K, Tohyama M, Katayama T (2012) TRAP1 controls mitochondrial fusion/fission balance through Drp1 and Mff expression. PLoS One 7:e51912 Takei K, Slepnev VI, Haucke V, De Camilli P (1999) Functional partnership between amphiphysin and dynamin in clathrin-mediated endocytosis. Nat Cell Biol 1(1):33–39 van Nies P, Nourian Z, Kok M, van Wijk R, Moeskops J, Westerlaken I, Poolman JM, Eelkema R, van Esch JH, Kuruma Y, Ueda T, Danelon C (2013) Unbiased tracking of the progression of mRNA and protein synthesis in bulk and inside lipid vesicles. ChemBioChem 14(15):1963–1966 Walde P (2010) Building artificial cells and protocell models: experimental approaches with lipid vesicles. Bioessays 32(4):296–303 Wick R, Luisi PL (1996) Enzyme-containing liposomes can endogenously produce membrane-constituting lipids. Chem Biol 3(4):277–285 Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95(12):6854–6859 Wollert T, Hurley JH (2010) Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464(7290):864–869 Wollert T, Wunder C, Lippincott-Schwartz J, Hurley JH (2009) Membrane scission by the ESCRT-III complex. Nature 458(7235):172–177 Yin Y, Arkhipov A, Schulten K (2009) Simulations of membrane tubulation by lattices of amphiphysin N-BAR domains. Structure 17(6):882–892 Zhao H, Pykäläinen A, Lappalainen P (2011) I-BAR domain proteins: linking actin and plasma membrane dynamics. Curr Opin Cell Biol 23(1):14–21 Zimmerberg J, Kozlov MM (2006) How proteins produce cellular membrane curvature. Nat Rev Mol Cell Biol 7(1):9–19