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The Heuristic of Form: Mitochondrial Morphology and the Explanation of Oxidative Phosphorylation

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Abstract

In the 1950s and 1960s, the search for the mechanism of oxidative phosphorylation by biochemists paralleled the description of mitochondrial form by George Palade and Fritiof Sjöstrand using electron microscopy. This paper explores the extent to which biochemists studying oxidative phosphorylation took mitochondrial form into account in the formulation of hypotheses, design of experiments, and interpretation of results. By examining experimental approaches employed by the biochemists studying oxidative phosphorylation, and their interactions with Palade, I suggest that use of mitochondrial form as a guide to experimentation and interpretation varied considerably among investigators. Most notably, Peter Mitchell, whose chemiosmotic hypothesis was ultimately the basis of the correct mechanism of oxidative phosphorylation, incorporated crucial aspects of mitochondrial form into his model that others failed to recognize. I discuss these historical observations in terms of the background and training of the biochemists, as well as a proposed heuristic of form, whose use may increase the possibility that biologically meaningful molecular mechanisms will be discovered.

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References

  • Allchin, D. 1991. Resolving Disagreement in Science: The Ox-Phos Controversy, 1961–1977. Chicago: University of Chicago.

  • Allchin, D. 1996. “Cellular and Theoretical Chimeras: Piecing Together How Cells Process Energy.” Studies in History and Philosophy of Science 27(1): 31–41.

    Article  Google Scholar 

  • Allchin, D. 1997. “A Twentieth-Century Phlogiston: Constructing Error and Differentiating Domains.” Perspectives on Science 5(1): 81–127.

    Google Scholar 

  • Allchin, D. 2002. “To Err and Win a Nobel Prize: Paul Boyer, ATP Synthase and the Emergence of Bioenergetics.” Journal of the History of Biology 35: 149–172.

    Article  Google Scholar 

  • Alsop, G.B. and Zhang, D. 2003. “Microtubules are the Only Structural Constituent of the Spindle Apparatus Required for Induction of Cell Cleavage.” Journal of Cell Biology 162(3): 383–390.

    Article  Google Scholar 

  • Anfinsen, Jr., C.B. 1957. “Structural Basis of Ribonuclease Activity.” Federation Proceedings 16: 783–791.

    Google Scholar 

  • Azzone, G.F. and Ernster, L. 1961. “Respiratory Control and Compartmentation of Substrate Level Phosphorylation of Liver Mitochondria.” Journal of Biological Chemistry 236: 1501–1509.

    Google Scholar 

  • Bearn, A.G. and James, D.G. 1978. “Dr. William Harvey (1578–1657) and the Harvey Society of New York.” Perspectives in Biology and Medicine 21(4): 524–535.

    Article  Google Scholar 

  • Bechtel, W. 1986. “Biochemistry: A Cross-Disciplinary Endeavor that Discovered a Distinctive Domain.” W. Bechtel (ed.), Integrating Scientific Disciplines. Dordrecht: Martinus Nijhoff, pp. 77–100.

    Chapter  Google Scholar 

  • Bechtel, W. 2006. Discovering Cell Mechanisms. Cambridge: Cambridge University Press.

    Google Scholar 

  • Bechtel, W. and Abrahamsen, A. 2007. “In Search of Mitochondrial Mechanisms: Interfield Excursions Between Cell Biology and Biochemistry.” Journal of the History of Biology 40(1): 1–33. doi:10.1007/s10739-006-9103-7.

    Article  Google Scholar 

  • Bechtel, W. and Richardson, R.C. 1993. Discovering Complexity. Princeton, New Jersey: Princeton University Press.

    Google Scholar 

  • Bechtel, W. 2011. “Mechanism and Biological Explanation.” Philosophy of Science 78(4): 533–557. doi:10.1086/661513.

    Article  Google Scholar 

  • Beinert, H., Stumpf, P.K., and Wakil, S.J. 2004. “David Ezra Green.” Biographical Memoirs of the National Academy 84: 1–34.

    Google Scholar 

  • Blobel, G. and Dobberstein, B. 1975a. “Transfer of Proteins Across Membranes. I. Presence of Proteolytically Processed and Unprocessed Nascent Immunoglobulin Light Chains on Membrane-Bound Ribosomes of Murine Myeloma.” Journal of Cell Biology 67(3): 835–851.

    Article  Google Scholar 

  • Blobel, G, Dobberstein, B. 1975b. “Transfer of Proteins Across Membranes. II. Reconstitution of Functional Rough Microsomes from Heterologous Components.” Journal of Cell Biology 67(3): 852–862.

    Article  Google Scholar 

  • Brigandt, I. and Love, A. 2012. “Reductionism in Biology.” E.N. Zalta (ed.), Stanford Encyclopedia of Philosophy. Palo Alto.

  • Bull, H.B. 1949. “Protein Denaturation.” R.A Gortner, Jr. and W.A. Gortner (eds.), Outlines of Biochemistry. New York: Wiley, pp. 439–447.

    Google Scholar 

  • Bull, H.B. and Neurath, H. 1937. “The Denaturation and Hydration of Proteins: II. Surface Denaturation of Egg Albumin.” The Journal of biological chemistry 118(1): 163–175.

    Google Scholar 

  • Claude, A. 1948. “Studies on Cells: Morphology, Chemical Constitution, and Distribution of Biochemical Functions.” Harvey Lectures 43: 121–164.

    Google Scholar 

  • Cooper, C., Devlin, T.M., and Lehninger, A.L. 1955. “Oxidative Phosphorylation in an Enzyme Fraction from Mitochondrial Extracts.” Biochimica et Biophysica Acta 18(1): 159–160.

    Article  Google Scholar 

  • Cowdry, E.V. 1924. General Cytology. Chicago: University of Chicago Press.

    Google Scholar 

  • Crane, F.L., Glenn, J.L., and Green, D.E. 1956. “Studies on the Electron Transfer System. IV. The Electron Transfer Particle.” Biochimica et Biophysica Acta 22(3): 475–487.

    Article  Google Scholar 

  • Crook, E.M. 1959. Structure and Function of Subcellular Components. Cambridge: Cambridge University Press.

    Google Scholar 

  • Danielli, J.F. 1975. “The Bilayer Hypothesis of Membrane Structure.” G. Weissmann and R. Claiborne (eds.), Cell Membranes. New York: HP Publishing, pp. 3–12.

    Google Scholar 

  • Davson, H. and Danielli, J.F. 1943. The Permeability of Natural Membranes. Cambridge: Cambridge University Press.

    Google Scholar 

  • Ernster, L. 1956. “Organization of Mitochondrial DPN-Linked Enzyme Systems.” Experimental Cell Research 10: 721–732.

    Article  Google Scholar 

  • Ernster, L. and Lindberg, O. 1958. “Animal Mitochondria.” Annual Review of Physiology 20(1): 13–40.

    Article  Google Scholar 

  • Ernster, L., Siekevitz, P., and Palade, G.E. 1962. “Enzyme–Structure Relationships in the Endoplasmic Reticulum of Rat Liver: A Morphological and Biochemical Study.” Journal of Cell Biology 15(3): 541–562.

    Article  Google Scholar 

  • Fernández-Morán, H. 1962. “Cell-Membrane Ultrastructure: Low-Temperature Electron Microsopy and X-ray Diffraction Studies of Lipoprotein Components in Lamellar Systems.” Circulation 26(5): 1039–1065. doi:10.1161/01.CIR.26.5.1039.

    Article  Google Scholar 

  • Fernández-Morán, H., Oda, T., Blair, P.V., and Green, D.E. 1964. “A Macromolecular Repeating Unit of Mitochondrial Structure and Function; Correlated Electron Microscopic and Biochemical Studies of Isolated Mitochondria and Submitochondrial Particles of Beef Heart Muscle.” Journal of Cell Biology 22: 63–100.

    Article  Google Scholar 

  • Green, D.E. 1937. “Reconstruction of the Chemical Events in Living Cells.” J. Needham and D.E. Green (eds.), Perspectives in Biochemistry. Cambridge: Cambridge University Press, pp. 175–186.

    Google Scholar 

  • Green, D.E. 1940. Mechanisms of Biological Oxidations. Cambridge: Cambridge University Press.

    Google Scholar 

  • Green, D.E. 1956–1958. Studies in Organized Enzyme Systems. Harvey Lectures 52: 177–227.

  • Green, D.E. 1962. “Structure and Function of Subcellular Particles.” Comparative Biochemistry and Physiology 4: 81–122.

    Article  Google Scholar 

  • Green, D.E., Haard, N.F., Lenaz, G., and Silman, H.I. 1968. “On the Noncatalytic Proteins of Membrane Systems.” Proceedings of the National Academy of Sciences of the United States of America 60: 277–284.

    Article  Google Scholar 

  • Green, D.E., Lester, R.L., and Ziegler, D.M. 1957. “Studies on the Mechanism of Oxidative Phosphorylation. I. Preparation and Properties of a Phosphorylating Electron Transfer Particle from Beef Heart Mitochondria.” Biochimica et Biophysica Acta 23(3): 516–524.

    Article  Google Scholar 

  • Green, D.E., Loomis, W.F., and Auerbach, V.H. 1948. “Studies on the Cyclophorase System; The Complete Oxidation of Pyruvic Acid to Carbon Dioxide and Water.” The Journal of Biological Chemistry 172(2): 389–403.

    Google Scholar 

  • Green, D.E., Tisdale, H.D., Criddle, R.S., Chen, P.Y., and Bock, R.M. 1961. “Isolation and Properties of the Structural Protein of Mitochondria.” Biochemical and Biophysical Research Communications 5: 109–114.

    Article  Google Scholar 

  • Green, D.E., Wharton, D.C., Tzagoloff, A., Rieske, J.S., and Brierley, G.P. 1965. “The Mitochondrial Electron Transport Chain.” T.E. King, H.S. Mason, and M. Morrison (eds.), Oxidases and Related Redox Systems. New York: Wiley, pp. 1032–1076.

    Google Scholar 

  • Harman, J.W. 1950a. “Studies on Mitochondria: I. The Association of Cyclophorase with Mitochondria.” Experimental Cell Research 1(3): 382–393.

    Article  Google Scholar 

  • Harman, J.W. 1950b. “Studies on Mitochondria: II. The Structure of Mitochondria in Relation to Enzymatic Activity.” Experimental Cell Research 1(3): 394–402.

    Article  Google Scholar 

  • Hogeboom, G.H., Claude, A., and Hotchkiss, R.D. 1946. “The Distribution of Cytochrome Oxidase and Succinoxidase in the Cytoplasm of the Mammalian Liver Cell.” The Journal of Biological Chemistry 165(2): 615–629.

    Google Scholar 

  • Hogeboom, G.H., Schneider, W.C., and Pallade, G.E. 1947. “The Isolation of Morphologically Intact Mitochondria from Rat Liver.” Proceedings of the Society for Experimental Biology and Medicine 65: 320–321.

    Article  Google Scholar 

  • —— 1948. Cytochemical studies of mammalian tissues. I. Isolation of Intact Mitochondria from Rat Liver; Some Biochemical Properties of Mitochondria and Submicroscopic Particulate Material. The Journal of Biological Chemistry 172(2): 619–635.

  • Jablonka, E. and Lamb, M.J. 2006. Evolution in Four Dimensions. Cambridge, Massachusetts: MIT Press.

    Google Scholar 

  • Kagawa, Y. and Racker, E. 1966a. “Partial Resolution of the Enzymes Catalyzing Oxidative Phosphorylation VIII. Properties of a Factor Conferring Oligomycin Sensitivity on Mitochondrial Adenosine Triphosphatase.” The Journal of Biological Chemistry 241(10): 2461–2466.

    Google Scholar 

  • Kagawa, Y. and Racker, E. 1966b. “Partial Resolution of the Enzymes Catalyzing Oxidative Phosphorylation. X. Correlation of Morphology and Function in Submitochondrial Particles.” The Journal of Biological Chemistry 241(10): 2475–2482.

    Google Scholar 

  • Kennedy, E.P. and Lehninger, A.L. 1948. “Intracellular Structures and the Fatty Acid Oxidase System of Rat Liver.” The Journal of Biological Chemistry 172(2): 847–848.

    Google Scholar 

  • Kennedy, E.P. and Lehninger, A.L. 1949. “Oxidation of Fatty Acids and Tricarboxylic Acid Intermediates by Isolated Rat Liver Mitochondria.” Journal of Biological Chemistry 179: 957–972.

    Google Scholar 

  • Knox, W.E., Noyce, B.N., and Auerbach, V.H. 1948. “Studies on the Cyclophorase System; Obligatory Sparking of Fatty Acid Oxidation.” Journal of Biological Chemistry 176(1): 117–122.

    Google Scholar 

  • Kohler, R.E. 1982. From Medical Chemistry to Biochemistry. Cambridge: Cambridge University Press.

    Book  Google Scholar 

  • Kresge, N., Simoni, R.D., and Hill, R.L. 2004. “Britton Chance: Olympian and Developer of Stop-Flow Methods.” The Journal of Biological Chemistry 279(50): e10–e10.

    Google Scholar 

  • Lehninger, A.L. 1959. “Reversal of Various Types of Mitochondrial Swelling by Adenosine Triphosphate.” The Journal of Biological Chemistry 234: 2465–2471.

    Google Scholar 

  • Lehninger, A.L. 1960. “The Enzymic and Morphologic Organization of the Mitochondria.” Pediatrics 26: 466–475.

    Google Scholar 

  • Lehninger, A.L. 1965. The Mitochondrion. New York: W. A. Benjamin.

    Google Scholar 

  • Lehninger, A.L., Wadkins, C.L., Cooper, C., Devlin, T.M., and Gamble, J.L. 1958. “Oxidative Phosphorylation.” Science 128(3322): 450–456.

    Article  Google Scholar 

  • Lehninger, A.L. 1955. “Oxidative Phosphorylation.” Harvey Lectures 49: 176–215.

    Google Scholar 

  • Levy, A. and Bechtel, W. 2013. “Abstraction and the Organization of Mechanisms.” Philosophy of Science 80(2): 241–261. doi:10.1086/670300.

    Article  Google Scholar 

  • Loeb, J. 1916. The Organism as a Whole. New York: G. P. Putnam’s and Sons.

    Google Scholar 

  • Maienschein, J. 1991. “From Presentation to Representation in E. B. Wilson’s the Cell.” Biology and Philosophy 6(2): 227–254. doi:10.1007/BF02426839.

    Article  Google Scholar 

  • Matlin, K.S. 2011. “Spatial Expression of the Genome: The Signal Hypothesis at Forty.” Nature Reviews Molecular Cell Biology 12(5): 333–340. doi:10.1038/nrm3105.

    Article  Google Scholar 

  • Mitchell, P. 1957. “Structure and Function of Subcellular Components.” Nature 179(4561): 661–662.

    Article  Google Scholar 

  • Mitchell, P. 1959a. “Biochemical Cytology of Microorganisms.” Annual Reviews in Microbiology 13(1): 407–440.

    Article  Google Scholar 

  • Mitchell, P. 1959b. “Structure and Function in Microorganisms.” E.M. Crook (ed.), Biochemical Society Symposium: The Structure and Function of Subcellular Components. Cambridge: Cambridge University Press, pp. 73–93.

    Google Scholar 

  • Mitchell, P. 1961a. “Approaches to the Analysis of Specific Membrane Transport.” T.W. Goodwin and O. Lindberg (eds.), Biological Structure and Function. New York: Academic Press, pp. 581–603.

    Google Scholar 

  • Mitchell, P. 1961b. “Biological Transport Phenomena and the Spatially Anisotropic Characteristics of Enzyme Systems Cause a Vector Component of Metabolism.” A. Kleinzeller and A. Kotyk (eds.), Membrane Transport and Metabolism. London: Academic Press, pp. 22–34.

    Google Scholar 

  • Mitchell, P. 1961c. “Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic Type of Mechanism.” Nature 191: 144–148.

    Article  Google Scholar 

  • Mitchell, P. 1966a. Chemiosmotic Coupling in Oxidative and Photosynthetic Phosphorylation. Bodmin, Cornwall: Glynn Research Ltd.

    Google Scholar 

  • Mitchell, P. 1966b. “Chemiosmotic Coupling in Oxidative and Photosynthetic Phosphorylation.” Biological Reviews of the Cambridge Philosophical Society 41(3): 445–502.

    Article  Google Scholar 

  • Mitchell, P. 1978. David Keilin’s Respiratory Chain Concept and Its Chemiosmotic Consequences. Nobel Lecture: 1–36.

  • Moberg, C. 2012. Entering an Unseen World. New York: The Rockefeller University Press.

    Google Scholar 

  • Moss, L. 2003. What Genes Can’t Do. Cambridge, Massachusetts: MIT Press.

    Google Scholar 

  • Mun, J.Y., Lee, T.H., Kim, J.H., Yoo, B.H., Bahk, Y.Y., Koo, H.-S., and Han, S.S. 2010. “Caenorhabditis elegans Mitofilm Homologs Control the Morphology of the Mitochondrial Cristae and Influence Reproduction and Physiology.” Journal of Cellular Physiology 224: 748–756.

    Article  Google Scholar 

  • Needham, J. 1942. Biochemistry and Morphogenesis. Cambridge: Cambridge University Press.

    Google Scholar 

  • Needham, J. 1949. Hopkins and Biochemistry. Cambridge: W. Heffer and Sons Ltd.

    Google Scholar 

  • Neurath, H., Greenstein, J.P., and Putnam, F.W. 1944. “The Chemistry of Protein Denaturation.” Chemical Reviews 34: 157–265.

    Article  Google Scholar 

  • Olby, R.C. 1994. The Path to the Double Helix. New York: Dover Publications.

    Google Scholar 

  • Palade, G.E. 1952a. “The Fine Structure of mitochondria.” Anatomical Record 114(3): 427–451.

    Article  Google Scholar 

  • Palade, G.E. 1952b. “A Study of Fixation for Electron Microscopy.” Journal of Experimental Medicine 95(3): 285–298.

    Article  Google Scholar 

  • Palade, G.E. 1953. “An Electron Microscope Study of the Mitochondrial Structure.” Journal of Histochemistry and Cytochemistry 1(4): 188–211. doi:10.1177/1.4.188.

    Article  Google Scholar 

  • Palade, G.E. 1956a. “Electron Microscopy of Mitochondria and Other Cytoplasmic Structures.” O.H Gaebler (ed.), Enzymes: Units of Biological Structure and Function. New York: Academic Press, pp. 185–215.

    Google Scholar 

  • Palade, G.E. 1956b. “The Fixation of Tissues for Electron Microscopy.” Proceedings of the Third International Conference on Electron Microscopy. London: Royal Microscopical Society.

  • Parks, W.G. 1962. “Gordon Research Conferences.” Science 135(3507): 932–944.

    Article  Google Scholar 

  • Parsons, D.F., Williams, G.R., and Chance, B. 1966. “Characteristics of Isolated and Purified Preparations of the Outer and Inner Membranes of Mitochondria.” Annals of the New York Academy of Sciences 137(2): 643–666.

    Article  Google Scholar 

  • Pauling, L., Corey, RB., and Branson, H.R. 1951. “The Structure of Proteins: Two Hydrogen-Bonded Helical Configurations of the Polypeptide Chain.” Proceedings of the National Academy of Sciences of the United States of America 37(4): 205–211.

    Article  Google Scholar 

  • Porter, K.R. and Bennett, H.S. 1981. Recollections on the Beginnings of the Journal of Cell Biology. The Journal of Cell Biology 91(3, Part 2): ix–xi.

  • Porter, K.R., Claude, A., and Fullam, E.F. 1945. “A Study of Tissue Culture Cells by Electron Microscopy: Methods and Preliminary Observations.” Journal of Experimental Medicine 81(3): 233–246.

    Article  Google Scholar 

  • Potter, V. 1956. “Added Comment.” O.H. Gaebler (ed.), Enzymes: Units of Biological Structure and Function. New York: Academic Press, pp. 252–256.

    Google Scholar 

  • Prebble, J. and Weber, B. 2003. Wandering in the Gardens of the Mind. Oxford: Oxford University Press.

    Google Scholar 

  • Prebble, J. 2001. “The Philosophical Origins of Mitchell’s Chemiosmotic Concepts: The Personal Factor in Scientific Theory Formulation.” Journal of the History of Biology 34(3): 433–460.

    Article  Google Scholar 

  • Pullman, M.E., Penefsky, H., and Racker, E. 1958. “A Soluble Protein Fraction Required for Coupling Phosphorylation to Oxidation in Submitochondrial Fragments of Beef Heart Mitochondria.” Archives of Biochemistry and Biophysics 76(1): 227–230.

    Article  Google Scholar 

  • Pullman, M.E., Penefsky, H.S., Datta, A., and Racker, E. 1960. “Partial Resolution of the Enzymes Catalyzing Oxidative Phosphorylation. I. Purification and Properties of Soluble Dinitrophenol-Stimulated Adenosine Triphosphatase.” The Journal of Biological Chemistry 235: 3322–3329.

    Google Scholar 

  • Racker, E. 1976. A New Look at Mechanisms in Bioenergetics. New York: Academic Press.

    Google Scholar 

  • Racker, E. and Gatt, S. 1959. “Interactions of Glycolysis and Oxidative Pathways.” Annals of the New York Academy of Sciences 72(12): 427–438.

    Article  Google Scholar 

  • Racker, E. and Stoeckenius, W. 1974. “Reconstitution of Purple Membrane Vesicles Catalyzing Light-Driven Proton Uptake and Adenosine Triphosphate Formation.” The Journal of Biological Chemistry 249(2): 662–663.

    Google Scholar 

  • Rasmussen, N. 1995. “Mitochondrial Structure and the Practice of Cell Biology in the 1950s.” Journal of the History of Biology 28(3): 381–429.

    Article  Google Scholar 

  • Rasmussen, N. 1997. Picture Control. Stanford, California: Stanford University Press.

    Google Scholar 

  • Robertson, J.D. 1959. “The Ultrastructure of Cell Membranes and Their Derivatives.” E.M. Crook (ed.), Biochemical Society Symposium: The Structure and Function of Subcellular Components. Cambridge: Cambridge University Press, pp. 3–43.

    Google Scholar 

  • Robinson, J.D. 1997. Moving Questions: A History of Membrane Transport and Bioenergetics. New York: Oxford University Press.

    Book  Google Scholar 

  • Rothman, J. and Fries, E. 1981. “Transport of Newly Synthesized Vesicular Stomatitis Viral Glycoprotein to Purified Golgi Membranes.” Journal of Cell Biology 89(1): 162–168.

    Article  Google Scholar 

  • Schatz, G. 1996. “Efraim Racker: June 28, 1913–September 9, 1991.” Biographical Memoirs – National Academy of Sciences 70: 321–346.

    Google Scholar 

  • Schneider, W.C. 1948. “Intracellular Distribution of Enzymes III. The Oxidation of Octanoic Acid by Rat Liver Fractions.” The Journal of Biological Chemistry 176(1): 259–266.

    Google Scholar 

  • Schneider, W.C. and Hogeboom, G.H. 1951. “Chemical Studies of Mammalian Tissues; The Isolation of Cell Components by Differential Centrifugation; A Review.” Cancer Research 11: 1–22.

    Google Scholar 

  • Siekevitz, P. 1983. “The Continuing Life of the Enzyme Club of New York City: The Growth of American Biochemistry from 1942 to 1982.” Transactions of the New York Academy of Sciences 41: 213–232.

    Article  Google Scholar 

  • Siekevitz, P. 1959. “On the Meaning of Intracellular Structure for Metabolic Regulation.” G.E.W. Wolstenholme and C.M. O’Connor (eds.), Regulation of Cell Metabolism. London: J. and A. Churchill Ltd., pp. 17–49.

    Google Scholar 

  • Siekevitz, P., Low, H., Ernster, L., and Lindberg, O. 1958. “On a Possible Mechanism of the Adenosinetriphosphatase of Liver Mitochondria.” Biochimica et Biophysica Acta 29(2): 378–391.

    Article  Google Scholar 

  • Siekevitz, P. and Watson, M.L. 1956a. “Cytochemical Studies of Mitochondria. I. The Separation and Identification of a Membrane Fraction from Isolated Mitochondria.” The Journal of Biophysical and Biochemical Cytology 2(6): 639–652.

    Article  Google Scholar 

  • Siekevitz, P. and Watson, M.L. 1956b. “Cytochemical Studies of Mitochondria. II. Enzymes Associated with a Mitochondrial Membrane Fraction.” The Journal of Biophysical and Biochemical Cytology 2(6): 653–669.

    Article  Google Scholar 

  • Siekevitz, P. and Watson, M.L. 1957. “Some Cytochemical Characteristics of a Phosphorylating Digitonin Preparation of Mitochondria.” Biochimica et Biophysica Acta 25(2): 274–279.

    Article  Google Scholar 

  • Sjöstrand, F.S. 1953. “Electron Microscopy of Mitochondria and Cytoplasmic Double Membranes.” Nature 171: 30–32.

    Article  Google Scholar 

  • Sjöstrand, F.S. 1955. The Ultrastructure of Mitochondria. In Fine Structure of Cells: Symposium Held the VIIIth Congress of Cell Biology. Leiden: Interscience Publishers, pp. 16–30.

  • Slater, E.C. 1953. “Mechanism of Phosphorylation in the Respiratory Chain.” Nature 172(4387): 975–978.

    Article  Google Scholar 

  • Slater, E.C. 2003. “Keilin, Cytochrome, and the Respiratory Chain.” Journal of Biological Chemistry 278(19): 16455–16461. doi:10.1074/jbc.X200011200.

    Article  Google Scholar 

  • Talalay, P. and Lane, M.D. 1986. “Albert Lester Lehninger 1917–1986.” Trends in Biochemical Sciences 11: 356–358.

    Article  Google Scholar 

  • Tzagoloff, A. 1982. Mitochondria. New York: Plenum Press.

    Google Scholar 

  • Voet, D. and Voet, J.G. 1995. Biochemistry, 2nd ed. New York: Wiley.

    Google Scholar 

  • Wagner, G.P. and Laubichler, M.D. 2000. “Character Identification in Evolutionary Biology: The Role of the Organism.” Theory in Biosciences 119: 20–40.

    Article  Google Scholar 

  • Warburg, O. 1913. “Über sauerstoffatmende Körnchen aus Leberzellen und Über Sauerstoffatmung in Berkefeld-Filtraten wässriger Leberextrackte.” PflÜgers Archiv: European Journal of Physiology 154: 599–617.

    Article  Google Scholar 

  • Weber, B.H. 1991. “Glynn and the Conceptual Development of the Chemiosmotic Theory: A Retrospective and Prospective View.” Bioscience Reports 11(6): 577–617.

    Article  Google Scholar 

  • Wimsatt, W.C. 1980. “Reductionistic Research Strategies and Their Biases in the Units of Selection Controversy.” T. Nickels (ed.), Scientific Discovery: Case Studies. Dordrecht: D. Reidel, pp. 213–259.

    Chapter  Google Scholar 

  • Wimsatt, W.C. 1997. “Aggregativity: Reductive Heuristics for Finding Emergence.” Philosophy of Science 64: S372–S384.

    Article  Google Scholar 

  • Wimsatt, W.C. 2007. Re-engineering Philosophy for Limited Beings. Cambridge, Massachusetts: Harvard University Press.

    Google Scholar 

  • Ziegler, D., Lester, R., and Green, D.E. 1956. “Oxidative Phosphorylation by an Electron Transport Particle from Beef Heart.” Biochimica et Biophysica Acta 21(1): 80–85.

    Article  Google Scholar 

  • Ziegler, D.M., Linnane, A.W., Green, D.E., Dass, C.M., and Ris, H. 1958. “Studies on the Electron Transport System. XI. Correlation of the Morphology and Enzymic Properties of Mitochondrial and Sub-Mitochondrial Particles.” Biochimica et Biophysica Acta 28(3): 524–538.

    Article  Google Scholar 

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  1. Department of Surgery and Committee on Conceptual and Historical Studies of Science, The University of Chicago, 5841 South Maryland Avenue, MC 5032, SBRI J557, Chicago, IL, 60637, USA

    Karl S. Matlin

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Matlin, K.S. The Heuristic of Form: Mitochondrial Morphology and the Explanation of Oxidative Phosphorylation. J Hist Biol 49, 37–94 (2016). https://doi.org/10.1007/s10739-015-9418-3

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