Home LiteratureArticle Details
PMID: 16339735 Published · ppublish English Journal Article Review

Molecules into cells: specifying spatial architecture.

Microbiology and molecular biology reviews : MMBR ·Vol. 69 ·No. 4 ·2005-12-00 ·Pages 544-64

Harold FM

Abstract

A living cell is not an aggregate of molecules but an organized pattern, structured in space and in time. This article addresses some conceptual issues in the genesis of spatial architecture, including how molecules find their proper location in cell space, the origins of supramolecular order, the role of the genes, cell morphology, the continuity of cells, and the inheritance of order. The discussion is framed around a hierarchy of physiological processes that bridge the gap between nanometer-sized molecules and cells three to six orders of magnitude larger. Stepping stones include molecular self-organization, directional physiology, spatial markers, gradients, fields, and physical forces. The knowledge at hand leads to an unconventional interpretation of biological order. I have come to think of cells as self-organized systems composed of genetically specified elements plus heritable structures. The smallest self that can be fairly said to organize itself is the whole cell. If structure, form, and function are ever to be computed from data at a lower level, the starting point will be not the genome, but a spatially organized system of molecules. This conclusion invites us to reconsider our understanding of what genes do, what organisms are, and how living systems could have arisen on the early Earth.

MeSH Terms
Bacteria/cytology,growth & development Cell Polarity Fungi/cytology,growth & development
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Harold Franklin M
Department of Microbiology, University of Washington, Seattle 98195, USA. frankharold@earthlink.net
References (128)
128 references, click to expand
  1. Cell polarity in yeast.
    Annu Rev Cell Dev Biol. 1999;15:365-91 PMID: 10611966
  2. Positional information in cells and organisms.
    Trends Cell Biol. 1992 Sep;2(9):256-60 PMID: 14731517
  3. Beyond molecules: self-assembly of mesoscopic and macroscopic components.
    Proc Natl Acad Sci U S A. 2002 Apr 16;99(8):4769-74 PMID: 11959929
  4. Polarity in action: asymmetric protein localization in bacteria.
    J Bacteriol. 2001 Jun;183(11):3261-7 PMID: 11344132
  5. The mitotic spindle: a self-made machine.
    Science. 2001 Oct 19;294(5542):543-7 PMID: 11641489
  6. A bacterial cell-cycle regulatory network operating in time and space.
    Science. 2003 Sep 26;301(5641):1874-7 PMID: 14512618
  7. The evolving complexity of cytoplasmic structure.
    Nat Rev Mol Cell Biol. 2002 Apr;3(4):291-6 PMID: 11994748
  8. Localization in the developing Fucus egg and the general role of localizing currents.
    Adv Morphog. 1968;7:295-328 PMID: 4881309
  9. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states.
    J Cell Sci. 2000 Feb;113 ( Pt 3):365-75 PMID: 10639324
  10. Yeasts make their mark.
    Nat Cell Biol. 2003 Apr;5(4):294-9 PMID: 12669083
  11. Matrix proteins can generate the higher order architecture of the Golgi apparatus.
    Nature. 2000 Oct 26;407(6807):1022-6 PMID: 11069184
  12. Turgor regulation in hyphal organisms.
    Fungal Genet Biol. 2004 Nov;41(11):1007-15 PMID: 15465389
  13. Causation and the origin of life. Metabolism or replication first?
    Orig Life Evol Biosph. 2004 Jun;34(3):307-21 PMID: 15068037
  14. Generating and exploiting polarity in bacteria.
    Science. 2002 Dec 6;298(5600):1942-6 PMID: 12471245
  15. Underlying assumptions of developmental models.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9372-7 PMID: 9689087
  16. Cellular oscillations and the regulation of growth: the pollen tube paradigm.
    Bioessays. 2001 Jan;23(1):86-94 PMID: 11135313
  17. Beyond self-assembly: from microtubules to morphogenesis.
    Cell. 1986 May 9;45(3):329-42 PMID: 3516413
  18. The Acid Growth Theory of auxin-induced cell elongation is alive and well.
    Plant Physiol. 1992 Aug;99(4):1271-4 PMID: 11537886
  19. Structural inheritance in Paramecium: ultrastructural evidence for basal body and associated rootlets polarity transmission through binary fission.
    Biol Cell. 2003 Jan-Feb;95(1):39-51 PMID: 12753952
  20. The new bacterial cell biology: moving parts and subcellular architecture.
    Cell. 2005 Mar 11;120(5):577-86 PMID: 15766522
  21. Resynthesizing evolutionary and developmental biology.
    Dev Biol. 1996 Feb 1;173(2):357-72 PMID: 8605997
  22. A protein interaction map for cell polarity development.
    J Cell Biol. 2001 Aug 6;154(3):549-71 PMID: 11489916
  23. The hardwiring of development: organization and function of genomic regulatory systems.
    Development. 1997 May;124(10):1851-64 PMID: 9169833
  24. Role of microtubules and tea1p in establishment and maintenance of fission yeast cell polarity.
    J Cell Sci. 2004 Feb 15;117(Pt 5):689-700 PMID: 14734657
  25. Surface tension-like forces determine bacterial shapes: Streptococcus faecium.
    J Gen Microbiol. 1981 Mar;123(1):151-61 PMID: 7320694
  26. Bacterial mitotic machineries.
    Cell. 2004 Feb 6;116(3):359-66 PMID: 15016371
  27. Cytoskeletal control of cell polarity in a plant zygote.
    Dev Biol. 1994 Oct;165(2):361-71 PMID: 7958406
  28. Mechanism of actin-based motility.
    Science. 2001 May 25;292(5521):1502-6 PMID: 11379633
  29. Self-organization of a propulsive actin network as an evolutionary process.
    Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11324-9 PMID: 11572984
  30. Dynamics and inheritance of the endoplasmic reticulum.
    J Cell Sci. 2004 Jun 15;117(Pt 14):2871-8 PMID: 15197242
  31. Self-assembly at all scales.
    Science. 2002 Mar 29;295(5564):2418-21 PMID: 11923529
  32. Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication.
    Proc Natl Acad Sci U S A. 2004 Jun 22;101(25):9257-62 PMID: 15178755
  33. Force and compliance: rethinking morphogenesis in walled cells.
    Fungal Genet Biol. 2002 Dec;37(3):271-82 PMID: 12431461
  34. Spontaneous cell polarization: undermining determinism.
    Nat Cell Biol. 2003 Apr;5(4):267-70 PMID: 12669070
  35. From morphogenes to morphogenesis.
    Microbiology. 1995 Nov;141 ( Pt 11):2765-78 PMID: 8535505
  36. Dynamic spatial regulation in the bacterial cell.
    Cell. 2000 Jan 7;100(1):89-98 PMID: 10647934
  37. Mapping the bacterial cell architecture into the chromosome.
    Philos Trans R Soc Lond B Biol Sci. 2000 Feb 29;355(1394):179-90 PMID: 10724454
  38. Calcium gradient dependence of Neurospora crassa hyphal growth.
    Microbiology. 2003 Sep;149(Pt 9):2475-2485 PMID: 12949173
  39. Polarity establishment requires dynamic actin in fucoid zygotes.
    Protoplasma. 2003 Jun;221(3-4):193-204 PMID: 12802626
  40. Tensegrity I. Cell structure and hierarchical systems biology.
    J Cell Sci. 2003 Apr 1;116(Pt 7):1157-73 PMID: 12615960
  41. Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell.
    Cell. 2003 Jun 13;113(6):767-76 PMID: 12809607
  42. Autopoiesis: a review and a reappraisal.
    Naturwissenschaften. 2003 Feb;90(2):49-59 PMID: 12590297
  43. The bacterial cytoskeleton: an intermediate filament-like function in cell shape.
    Cell. 2003 Dec 12;115(6):705-13 PMID: 14675535
  44. Themes and variations in prokaryotic cell division.
    FEMS Microbiol Rev. 2000 Oct;24(4):531-48 PMID: 10978550
  45. Polarized growth and organelle segregation in yeast: the tracks, motors, and receptors.
    J Cell Biol. 2003 Mar 17;160(6):811-6 PMID: 12642608
  46. A three-dimensional model of fungal morphogenesis based on the vesicle supply center concept.
    J Theor Biol. 2001 Jan 21;208(2):151-64 PMID: 11162061
  47. The expression of asymmetry during Caulobacter cell differentiation.
    Annu Rev Biochem. 1994;63:419-50 PMID: 7979244
  48. In defense of "nonmolecular" cell biology.
    Int Rev Cytol. 1990;120:191-241 PMID: 2406213
  49. On the crucial stages in the origin of animate matter.
    J Mol Evol. 1997 Jan;44(1):1-8 PMID: 9010131
  50. Linear ordering and dynamic segregation of the bacterial chromosome.
    Proc Natl Acad Sci U S A. 2004 Jun 22;101(25):9175-6 PMID: 15199189
  51. Genetics. Venter gets down to life's basics.
    Science. 2002 Nov 29;298(5599):1701 PMID: 12459564
  52. Bacterial cell division and the Z ring.
    Annu Rev Biochem. 1997;66:93-116 PMID: 9242903
  53. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):181-203 PMID: 9529891
  54. The driving force for life's emergence: kinetic and thermodynamic considerations.
    J Theor Biol. 2003 Feb 7;220(3):393-406 PMID: 12468287
  55. Cell cycle control of cell morphogenesis in Caulobacter.
    Curr Opin Microbiol. 2001 Dec;4(6):674-80 PMID: 11731319
  56. A new biology for a new century.
    Microbiol Mol Biol Rev. 2004 Jun;68(2):173-86 PMID: 15187180
  57. Cell polarity and morphogenesis in budding yeast.
    Annu Rev Microbiol. 1998;52:687-744 PMID: 9891811
  58. Symmetry breaking in the zygotes of the fucoid algae: controversies and recent progress.
    Curr Top Dev Biol. 1999;44:101-25 PMID: 9891878
  59. The bacterium's way for safe enlargement and division.
    Appl Environ Microbiol. 2000 Sep;66(9):3657-63 PMID: 10966373
  60. On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells.
    Philos Trans R Soc Lond B Biol Sci. 2003 Jan 29;358(1429):59-83; discussion 83-5 PMID: 12594918
  61. Bacterial cell division.
    Annu Rev Genet. 1999;33:423-48 PMID: 10690414
  62. Recruitment of a cytoplasmic response regulator to the cell pole is linked to its cell cycle-regulated proteolysis.
    Proc Natl Acad Sci U S A. 2004 May 11;101(19):7415-20 PMID: 15123835
  63. Morphogenesis of Escherichia coli.
    Microbiol Mol Biol Rev. 1998 Mar;62(1):110-29 PMID: 9529889
  64. Self-organization of sorted patterned ground.
    Science. 2003 Jan 17;299(5605):380-3 PMID: 12532013
  65. Bacterial shape.
    Mol Microbiol. 2003 Aug;49(3):571-80 PMID: 12914007
  66. Self-organization of microtubules and motors.
    Nature. 1997 Sep 18;389(6648):305-8 PMID: 9305848
  67. Polar explorers: membrane proteins that determine division site placement.
    Cell. 2001 Jul 13;106(1):13-6 PMID: 11461697
  68. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae.
    EMBO J. 1996 Dec 2;15(23):6483-94 PMID: 8978675
  69. Basal body/centriole assembly and continuity.
    Curr Opin Cell Biol. 2003 Feb;15(1):96-104 PMID: 12517710
  70. The multiprotein exocyst complex is essential for cell separation in Schizosaccharomyces pombe.
    Mol Biol Cell. 2002 Feb;13(2):515-29 PMID: 11854409
  71. An actin-like gene can determine cell polarity in bacteria.
    Proc Natl Acad Sci U S A. 2004 Jun 8;101(23):8643-8 PMID: 15159537
  72. Rethinking cell structure.
    Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5251-7 PMID: 7777493
  73. What determines growth direction in fungal hyphae?
    Fungal Genet Biol. 1998 Jun-Jul;24(1-2):101-9 PMID: 9742196
  74. Polarization of cell growth in yeast.
    J Cell Sci. 2000 Feb;113 ( Pt 4):571-85 PMID: 10652251
  75. Dynein and dynactin deficiencies affect the formation and function of the Spitzenkörper and distort hyphal morphogenesis of Neurospora crassa.
    Microbiology. 2000 Jul;146 ( Pt 7):1743-1752 PMID: 10878138
  76. Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area.
    Int Rev Cytol. 2000;192:189-221 PMID: 10553280
  77. Establishment of cell polarity in yeast.
    Cold Spring Harb Symp Quant Biol. 1995;60:729-44 PMID: 8824448
  78. Physical properties determining self-organization of motors and microtubules.
    Science. 2001 May 11;292(5519):1167-71 PMID: 11349149
  79. F-actin distribution and function during sexual differentiation in Schizosaccharomyces pombe.
    J Cell Sci. 1998 Apr;111 ( Pt 7):867-76 PMID: 9490631
  80. Polarity in filamentous fungi: moving beyond the yeast paradigm.
    Fungal Genet Biol. 2004 Apr;41(4):391-400 PMID: 14998522
  81. Biophysics of bacterial walls viewed as stress-bearing fabric.
    Microbiol Rev. 1988 Sep;52(3):337-53 PMID: 3054466
  82. Three-dimensional analysis of morphogenesis induced by mating pheromone alpha factor in Saccharomyces cerevisiae.
    J Cell Sci. 1989 Oct;94 ( Pt 2):207-16 PMID: 2695529
  83. Morphogenetic properties of microtubules and mitotic spindle assembly.
    Cell. 1996 Feb 9;84(3):401-10 PMID: 8608594
  84. Self-organization of treadmilling microtubules into a polar array.
    Trends Cell Biol. 2002 Oct;12(10):462-5 PMID: 12441249
  85. Spatial and temporal control of differentiation and cell cycle progression in Caulobacter crescentus.
    Annu Rev Microbiol. 2003;57:225-47 PMID: 14527278
  86. A journey into space.
    Nat Rev Mol Cell Biol. 2001 Sep;2(9):647-56 PMID: 11533722
  87. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis.
    Cell. 2001 Mar 23;104(6):913-22 PMID: 11290328
  88. More than one way to replicate the Golgi apparatus.
    Nat Cell Biol. 2002 Oct;4(10):E223-4 PMID: 12360298
  89. Fluorescence bleaching reveals asymmetric compartment formation prior to cell division in Caulobacter.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8235-40 PMID: 12824468
  90. Pattern formation in Escherichia coli: a model for the pole-to-pole oscillations of Min proteins and the localization of the division site.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14202-7 PMID: 11734639
  91. Identification of a localization factor for the polar positioning of bacterial structural and regulatory proteins.
    Proc Natl Acad Sci U S A. 2002 Oct 15;99(21):13831-6 PMID: 12370432
  92. New concepts in fission yeast morphogenesis.
    Philos Trans R Soc Lond B Biol Sci. 2000 Jul 29;355(1399):873-7 PMID: 11128980
  93. Morphogen gradient interpretation.
    Nature. 2001 Oct 25;413(6858):797-803 PMID: 11677596
  94. Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7865-70 PMID: 12766229
  95. Tensegrity II. How structural networks influence cellular information processing networks.
    J Cell Sci. 2003 Apr 15;116(Pt 8):1397-408 PMID: 12640025
  96. Metaphors and the role of genes in development.
    Bioessays. 1990 Sep;12(9):441-6 PMID: 1979486
  97. Membrane heredity and early chloroplast evolution.
    Trends Plant Sci. 2000 Apr;5(4):174-82 PMID: 10740299
  98. Establishment of a cellular axis in fission yeast.
    Trends Genet. 2001 May;17(5):273-8 PMID: 11335037
  99. The antiquity of RNA-based evolution.
    Nature. 2002 Jul 11;418(6894):214-21 PMID: 12110897
  100. Morphology, growth and reversion in a stable L-form of Escherichia coli K12.
    J Gen Microbiol. 1987 Mar;133(3):527-34 PMID: 3309159
  101. The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front.
    J Geol Soc London. 1997 May;154(3):377-402 PMID: 11541234
  102. Inheriting a structural scaffold for Golgi biosynthesis.
    Bioessays. 2002 Jul;24(7):584-7 PMID: 12111718
  103. Cytoskeletal and Ca2+ regulation of hyphal tip growth and initiation.
    Curr Top Dev Biol. 2001;51:135-87 PMID: 11236713
  104. Mapping the growth of fungal hyphae: orthogonal cell wall expansion during tip growth and the role of turgor.
    Biophys J. 2000 Nov;79(5):2382-90 PMID: 11053117
  105. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli.
    EMBO J. 2001 Apr 2;20(7):1563-72 PMID: 11285221
  106. The case for morphogens in plants.
    Nat Cell Biol. 2003 Nov;5(11):939-43 PMID: 14593411
  107. Yeast autophagosomes: de novo formation of a membrane structure.
    Trends Cell Biol. 2002 May;12(5):231-5 PMID: 12062171
  108. On the evolution of cells.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8742-7 PMID: 12077305
  109. Plasma membrane disruption: repair, prevention, adaptation.
    Annu Rev Cell Dev Biol. 2003;19:697-731 PMID: 14570587
  110. Do we understand development?
    Science. 1994 Oct 28;266(5185):571-2 PMID: 7939707
  111. To shape a cell: an inquiry into the causes of morphogenesis of microorganisms.
    Microbiol Rev. 1990 Dec;54(4):381-431 PMID: 2128368
  112. Toward self-organization and complex matter.
    Science. 2002 Mar 29;295(5564):2400-3 PMID: 11923524
  113. Spindle pole body duplication: a model for centrosome duplication?
    Trends Cell Biol. 2000 Aug;10(8):329-35 PMID: 10884685
  114. The concept of self-organization in cellular architecture.
    J Cell Biol. 2001 Oct 15;155(2):181-5 PMID: 11604416
  115. Regulation of the tip-high [Ca2+] gradient in growing hyphae of the fungus Neurospora crassa.
    Eur J Cell Biol. 2001 Jun;80(6):379-90 PMID: 11484929
  116. Cytokinesis in prokaryotes and eukaryotes: common principles and different solutions.
    Microbiol Mol Biol Rev. 2001 Jun;65(2):319-33 ; third page, table of contents PMID: 11381104
  117. The coming Kuhnian revolution in biology.
    Nat Biotechnol. 1997 Mar;15(3):194-200 PMID: 9062910
  118. Adaptation of core mechanisms to generate cell polarity.
    Nature. 2003 Apr 17;422(6933):766-74 PMID: 12700771
  119. Cytokinesis in bacteria.
    Microbiol Mol Biol Rev. 2003 Mar;67(1):52-65, table of contents PMID: 12626683
  120. The fission yeast microtubule cytoskeleton.
    J Cell Sci. 1998 Jun;111 ( Pt 12):1603-12 PMID: 9601091
  121. Dynamics and mechanics of the microtubule plus end.
    Nature. 2003 Apr 17;422(6933):753-8 PMID: 12700769
  122. Crawling toward a unified model of cell mobility: spatial and temporal regulation of actin dynamics.
    Annu Rev Biochem. 2004;73:209-39 PMID: 15189141
  123. Life without a cell membrane: regeneration of protoplasts from disintegrated cells of the marine green alga Bryopsis plumosa.
    J Cell Sci. 2001 Jun;114(Pt 11):2009-14 PMID: 11493637
  124. Morphogens: how big is the big picture?
    Nat Cell Biol. 2001 Jul;3(7):E151-4 PMID: 11433305
  125. Molecular "vitalism".
    Cell. 2000 Jan 7;100(1):79-88 PMID: 10647933
  126. Let there be life. Thermodynamic reflections on biogenesis and evolution.
    J Theor Biol. 1994 Jun 21;168(4):429-59 PMID: 8072301
  127. Obcells as proto-organisms: membrane heredity, lithophosphorylation, and the origins of the genetic code, the first cells, and photosynthesis.
    J Mol Evol. 2001 Oct-Nov;53(4-5):555-95 PMID: 11675615
  128. Loosening of plant cell walls by expansins.
    Nature. 2000 Sep 21;407(6802):321-6 PMID: 11014181
Article Info
Journal
Microbiology and molecular biology reviews : MMBR
Abbr.
Microbiol Mol Biol Rev
ISSN
1092-2172
Published
2005-12-00
Pages
544-64
Language
English
Region
United States
NLM ID
9706653
PMCID
PMC1306800
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com