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. 1962 Sep;41(9):1776–1804. doi: 10.1172/JCI104637

A CASE OF SEVERE HYPERMETABOLISM OF NONTHYROID ORIGIN WITH A DEFECT IN THE MAINTENANCE OF MITOCHONDRIAL RESPIRATORY CONTROL: A CORRELATED CLINICAL, BIOCHEMICAL, AND MORPHOLOGICAL STUDY

Rolf Luft 1,2,3,*, Denis Ikkos 1,2,3,*, Genaro Palmieri 1,2,3,*, Lars Ernster 1,2,3,†, Björn Afzelius 1,2,3,‡
PMCID: PMC291101  PMID: 14467237

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ANDRE J. [On the existence of a paracrystalline state of the chondriosomic material of certain spermatozoids]. C R Hebd Seances Acad Sci. 1959 Oct 5;249:1264–1266. [PubMed] [Google Scholar]
  2. ASBOE-HANSEN G., IVERSEN K., WICHMANN R. Malignant exophthalmos; muscular changes and thyrotrophin content in serum. Acta Endocrinol (Copenh) 1952 Dec;11(4):376–399. [PubMed] [Google Scholar]
  3. AZZONE G. F., EEG-OLOFSSON O., ERNSTER L., LUFT R., SZABOLCSI G. Studies on isolated human skeletal muscle mitochondria. Exp Cell Res. 1961 Jan;22:415–436. doi: 10.1016/0014-4827(61)90119-7. [DOI] [PubMed] [Google Scholar]
  4. BORELL U., NILSSON O., WESTMAN A. The cyclical changes occurring in the epithelium lining the endometrial glands: an electron-microscopical study in the human being. Acta Obstet Gynecol Scand. 1959;38:364–377. doi: 10.3109/00016345909157994. [DOI] [PubMed] [Google Scholar]
  5. BRODY I. An ultrastructural study on the role of the keratohyalin granules in the keratinization process. J Ultrastruct Res. 1959 Oct;3:84–104. doi: 10.1016/s0022-5320(59)80018-6. [DOI] [PubMed] [Google Scholar]
  6. CHAPPELL J. B., PERRY S. V. Biochemical and osmotic properties of skeletal muscle mitochondria. Nature. 1954 Jun 5;173(4414):1094–1095. doi: 10.1038/1731094a0. [DOI] [PubMed] [Google Scholar]
  7. DE HARVEN E., COERS C. Electron microscope study of the human neuromuscular junction. J Biophys Biochem Cytol. 1959 Aug;6(1):7–10. doi: 10.1083/jcb.6.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. EDWARDS G. A., RUSKA H., DE HARVEN E. Neuromuscular junctions in flight and tymbal muscles of the cicada. J Biophys Biochem Cytol. 1958 May 25;4(3):251–256. doi: 10.1083/jcb.4.3.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. EHRET C. F., MINICK O. T., POWERS E. L., ROTH L. E. The internal organization of mitochondria. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):341–346. doi: 10.1083/jcb.2.4.341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. ERNSTER L., IKKOS D., LUFT R. Enzymic activities of human skeletal muscle mitochondria: a tool in clinical metabolic research. Nature. 1959 Dec 12;184:1851–1854. doi: 10.1038/1841851a0. [DOI] [PubMed] [Google Scholar]
  11. ERNSTER L., JALLING O., LOW H., LINDBERG O. Alternative pathways of mitochondrial DPNH oxidation, studied with amytal. Exp Cell Res. 1955;(Suppl 3):124–132. [PubMed] [Google Scholar]
  12. ERNSTER L., LINDBERG O. Animal mitochondria. Annu Rev Physiol. 1958;20:13–42. doi: 10.1146/annurev.ph.20.030158.000305. [DOI] [PubMed] [Google Scholar]
  13. ERNSTER L. Organization of mitochondrial DPN-linked systems. II. Regulation of alternative electron transfer pathways. Exp Cell Res. 1956 Jun;10(3):721–732. doi: 10.1016/0014-4827(56)90049-0. [DOI] [PubMed] [Google Scholar]
  14. FAWCETT D. W. Observations on the cytology and electron microscopy of hepatic cells. J Natl Cancer Inst. 1955 Apr;15(5 Suppl):1475–1503. [PubMed] [Google Scholar]
  15. GLAUERT A. M., GLAUERT R. H., ROGERS G. E. A new embedding medium for electron microscopy. Nature. 1956 Oct 13;178(4537):803–803. doi: 10.1038/178803a0. [DOI] [PubMed] [Google Scholar]
  16. GRABE B. Electron distribution in some high energy phosphates and transfer of energy from catabolism to anabolism. Biochim Biophys Acta. 1958 Dec;30(3):560–569. doi: 10.1016/0006-3002(58)90103-3. [DOI] [PubMed] [Google Scholar]
  17. GROLLMAN A. Water and electrolyte content of tissues of the adrenalectomized and adrenalectomized-nephrectomized dog. Am J Physiol. 1954 Oct;179(1):36–38. doi: 10.1152/ajplegacy.1954.179.1.36. [DOI] [PubMed] [Google Scholar]
  18. HOLMGREN A., JONSSON B., LEVANDER M., LINDERHOLM H., SJOSTRAND T., STROM G. Low physical working capacity in suspected heart cases due to inadequate adjustment of peripheral blood flow (vasoregulatory asthenia). Acta Med Scand. 1957 Oct 15;158(6):413–436. doi: 10.1111/j.0954-6820.1957.tb15509.x. [DOI] [PubMed] [Google Scholar]
  19. HUIJING F., SLATER E. C. The use of oligomycin as an inhibitor of oxidative phosphorylation. J Biochem. 1961 Jun;49:493–501. doi: 10.1093/oxfordjournals.jbchem.a127334. [DOI] [PubMed] [Google Scholar]
  20. HUNTER F. E., Jr, FORD L. Inactivation of oxidative and phosphorylative systems in mitochondria by preincubation with phosphate and other ions. J Biol Chem. 1955 Sep;216(1):357–369. [PubMed] [Google Scholar]
  21. Hoch F. L., Lipmann F. THE UNCOUPLING OF RESPIRATION AND PHOSPHORYLATION BY THYROID HORMONES. Proc Natl Acad Sci U S A. 1954 Oct;40(10):909–921. doi: 10.1073/pnas.40.10.909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. JEZEQUEL A. M. [Myelin degeneration of the mitochondria of the human liver in epithelioma of the choledochus and in viral jaundice. Study with the electron microscope]. J Ultrastruct Res. 1959 Dec;3:210–215. doi: 10.1016/s0022-5320(59)90015-2. [DOI] [PubMed] [Google Scholar]
  23. LARAMORE D. C., GROLLMAN A. Water and electrolyte content of tissues in normal and hypertensive rats. Am J Physiol. 1950 May;161(2):278–282. doi: 10.1152/ajplegacy.1950.161.2.278. [DOI] [PubMed] [Google Scholar]
  24. LARDY H. A., JOHNSON D., McMURRAY W. C. Antibiotics as tools for metabolic studies. I. A survey of toxic antibiotics in respiratory, phosphorylative and glycolytic systems. Arch Biochem Biophys. 1958 Dec;78(2):587–597. doi: 10.1016/0003-9861(58)90383-7. [DOI] [PubMed] [Google Scholar]
  25. LARDY H. A., PRESSMAN B. C. Effect of surface active agents on the latent ATPase of mitochondria. Biochim Biophys Acta. 1956 Sep;21(3):458–466. doi: 10.1016/0006-3002(56)90182-2. [DOI] [PubMed] [Google Scholar]
  26. LARDY H. A., WELLMAN H. Oxidative phosphorylations; rôle of inorganic phosphate and acceptor systems in control of metabolic rates. J Biol Chem. 1952 Mar;195(1):215–224. [PubMed] [Google Scholar]
  27. LEHNINGER A. L. Oxidative phosphorylation. Harvey Lect. 1953;49:176–215. [PubMed] [Google Scholar]
  28. LEHNINGER A. L. Thyroxine and the swelling and contraction cycle in mitochondria. Ann N Y Acad Sci. 1960 Apr 23;86:484–493. doi: 10.1111/j.1749-6632.1960.tb42824.x. [DOI] [PubMed] [Google Scholar]
  29. LEVER J. D. Remarks on the electron microscopy of the rat luteum and comparison with earlier observations on the adrenal cortex. Anat Rec. 1956 Jan;124(1):111–125. doi: 10.1002/ar.1091240109. [DOI] [PubMed] [Google Scholar]
  30. LINDNER E. Die submikroskopische Morphologie des Herzmuskels. Z Zellforsch Mikrosk Anat. 1957;45(6):702–746. [PubMed] [Google Scholar]
  31. LOW H., SIEKEVITZ P., ERNSTER L., LINDBERG O. Studies on the relation of the adenosinetriphosphate-inorganic phosphate exchange reaction of mitochondria to oxidative phosphorylation. Biochim Biophys Acta. 1958 Aug;29(2):392–405. doi: 10.1016/0006-3002(58)90198-7. [DOI] [PubMed] [Google Scholar]
  32. LUFT J. H. Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol. 1961 Feb;9:409–414. doi: 10.1083/jcb.9.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. MOORE R. D., MUMAW V., SCHOENBERG M. D. Optical microscopy of ultrathin tissue sections. J Ultrastruct Res. 1960 Nov;4:113–116. doi: 10.1016/s0022-5320(60)90047-2. [DOI] [PubMed] [Google Scholar]
  34. MUSCATELLO U., ANDERSSON-CEDERGREN E., AZZONE G. F., von der DECKEN The sarcotubular system of frog skeletal muscle. A morphological and biochemical study. J Biophys Biochem Cytol. 1961 Aug;10(4):201–218. doi: 10.1083/jcb.10.4.201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Mudge G. H., Vislocky K. ELECTROLYTE CHANGES IN HUMAN STRIATED MUSCLE IN ACIDOSIS AND ALKALOSIS. J Clin Invest. 1949 May;28(3):482–486. doi: 10.1172/JCI102094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. NAPOLITANO L., FAWCETT D. The fine structure of brown adipose tissue in the newborn mouse and rat. J Biophys Biochem Cytol. 1958 Nov 25;4(6):685–692. doi: 10.1083/jcb.4.6.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. NILSSON O. Ultrastructure of mouse uterine surface epithelium under different estrogenic influences. 1. Spayed animals and oestrous animals. J Ultrastruct Res. 1958 Aug;1(4):375–396. doi: 10.1016/s0022-5320(58)90009-1. [DOI] [PubMed] [Google Scholar]
  38. PALADE G. E. An electron microscope study of the mitochondrial structure. J Histochem Cytochem. 1953 Jul;1(4):188–211. doi: 10.1177/1.4.188. [DOI] [PubMed] [Google Scholar]
  39. PALADE G. E. The fine structure of mitochondria. Anat Rec. 1952 Nov;114(3):427–451. doi: 10.1002/ar.1091140304. [DOI] [PubMed] [Google Scholar]
  40. POCHE R. Submikroskopische Beiträge zur Pathologie der Herzmuskelzelle bei Phosphorvergiftung, Hypertrophie, Atrophie und Kaliummangel. Virchows Arch Pathol Anat Physiol Klin Med. 1958;331(2):165–248. doi: 10.1007/BF00955194. [DOI] [PubMed] [Google Scholar]
  41. POLIS B. D., SHMUKLER H. W. Mitochrome. I. Isolation and physicochemical properties. II. Enzymatic effects. J Biol Chem. 1957 Jul;227(1):419–440. [PubMed] [Google Scholar]
  42. PORTER K. R., PALADE G. E. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol. 1957 Mar 25;3(2):269–300. doi: 10.1083/jcb.3.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. POTTER V. R., REIF A. E. Inhibition of an electron transport component by antimycin A. J Biol Chem. 1952 Jan;194(1):287–297. [PubMed] [Google Scholar]
  44. PULLMAN M. E., RACKER E. Spectrophotometric studies of oxidative phosphorylation. Science. 1956 Jun 22;123(3208):1105–1107. doi: 10.1126/science.123.3208.1105. [DOI] [PubMed] [Google Scholar]
  45. ROUILLER C. Physiological and pathological changes in mitochondrial morphology. Int Rev Cytol. 1960;9:227–292. doi: 10.1016/s0074-7696(08)62748-5. [DOI] [PubMed] [Google Scholar]
  46. RUDZINSKA M. A., SEDAR A. W. Mitochondria of protozoa. J Biophys Biochem Cytol. 1956 Jul 25;2(4 Suppl):331–336. doi: 10.1083/jcb.2.4.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. SABATINI D. D., DE ROBERTIS E. D. Ultrastructural zonation of adrenocortex in the rat. J Biophys Biochem Cytol. 1961 Jan;9:105–119. doi: 10.1083/jcb.9.1.105. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. SACKTOR B. Investigations on the mitochondria of the housefly, Musca domestica L. III. Requirements for oxidative phosphorylation. J Gen Physiol. 1954 Jan 20;37(3):343–359. doi: 10.1085/jgp.37.3.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. SEDAR A. W., PORTER K. R. The fine structure of cortical components of Paramecium multimicronucleatum. J Biophys Biochem Cytol. 1955 Nov 25;1(6):583–604. doi: 10.1083/jcb.1.6.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. SETALA K., MERENMIES L., NISKANEN E. E., NYHOLM M., STJERNVALL L. Mechanism of experimental tumorigenesis. VI. Ultrastructural alterations in mouse epidermis caused by locally applied carcinogen and dipole-type tumor promoter. J Natl Cancer Inst. 1960 Nov;25:1155–1189. [PubMed] [Google Scholar]
  51. SHELDON H., ZETTERQVIST H. Experimental induced changes in mitochondrial morphology: vitamin A deficiency. Exp Cell Res. 1956 Feb;10(1):225–228. doi: 10.1016/0014-4827(56)90089-1. [DOI] [PubMed] [Google Scholar]
  52. SIEKEVITZ P., WATSON M. L. Cytochemical studies of mitochondria. I. The separation and identification of a membrane fraction from isolated mitochondria. J Biophys Biochem Cytol. 1956 Nov 25;2(6):639–652. doi: 10.1083/jcb.2.6.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. SJOSTRAND F. S. A new microtome for ultrathin sectioning for high resolution electron microscopy. Experientia. 1953 Mar 15;9(3):114–115. doi: 10.1007/BF02178346. [DOI] [PubMed] [Google Scholar]
  54. TATA J. R., ERNSTER L., LINDBERG O. Control of basal metabolic rate by thyroid hormones and cellular function. Nature. 1962 Mar 17;193:1058–1060. doi: 10.1038/1931058a0. [DOI] [PubMed] [Google Scholar]
  55. TATA J. R. The partial purification and properties of thyroxine dehalogenase. Biochem J. 1960 Nov;77:214–226. doi: 10.1042/bj0770214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. TATA J. R. The physiological significance of thyroxine dehalogenase. Acta Endocrinol (Copenh) 1961 May;37:125–134. doi: 10.1530/acta.0.0370125. [DOI] [PubMed] [Google Scholar]
  57. VAN BREEMEN V. L. Ultrastructure of human muscle. I. Observations on normal striated muscle fibers. Am J Pathol. 1960 Aug;37:215–229. [PMC free article] [PubMed] [Google Scholar]
  58. VICKERMAN K. Structural changes in mitochondria of Acanthamoeba at encystation. Nature. 1960 Oct 15;188:248–249. doi: 10.1038/188248a0. [DOI] [PubMed] [Google Scholar]
  59. WATANABE M. I., WILLIAMS C. M. Mitochondria in the flight muscles of insects. II. Effects of the medium on the size form, and organization of isolated sarcosomes. J Gen Physiol. 1953 Sep;37(1):71–90. doi: 10.1085/jgp.37.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. WITTER R. F., WATSON M. L., COTTONE M. A. Morphology and ATP-ase of isolated mitochondria. J Biophys Biochem Cytol. 1955 Mar;1(2):127–138. doi: 10.1083/jcb.1.2.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. WOJTCZAK L., LEHNINGER A. L. Formation and disappearance of an endogenous uncoupling factor during swelling and contraction of mitochondria. Biochim Biophys Acta. 1961 Aug 19;51:442–456. doi: 10.1016/0006-3002(61)90600-x. [DOI] [PubMed] [Google Scholar]
  62. YAMADA E. A crystalline body found in the rod inner segment of the frog's eye. J Biophys Biochem Cytol. 1959 Dec;6:517–518. doi: 10.1083/jcb.6.3.517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. YOSHIMURA F., IRIE M. [Light and electron microscopic studies on crystalloids in thyroid cells]. Z Zellforsch Mikrosk Anat. 1961;55:204–219. [PubMed] [Google Scholar]

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