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Home / Equine Research Bank / Histochem Cell Biol / Giant crystals inside mitochondria of equine chondrocytes.
Histochemistry and cell biology2016; 147(5); 635-649; doi: 10.1007/s00418-016-1516-6

Giant crystals inside mitochondria of equine chondrocytes.

Abstract: The present study reports for the first time the presence of giant crystals in mitochondria of equine chondrocytes. These structures show dark contrast in TEM images as well as a granular substructure of regularly aligned 1-2 nm small units. Different zone axes of the crystalline structure were analysed by means of Fourier transformation of lattice-resolution TEM images proving the crystalline nature of the structure. Elemental analysis reveals a high content of nitrogen referring to protein. The outer shape of the crystals is geometrical with an up to hexagonal profile in cross sections. It is elongated, spanning a length of several micrometres through the whole cell. In some chondrocytes, several crystals were found, sometimes combined in a single mitochondrion. Crystals were preferentially aligned along the long axis of the cells, thus appearing in the same orientation as the chondrocytes in the tissue. Although no similar structures have been found in the cartilage of any other species investigated, they have been found in cartilage repair tissue formed within a mechanically stimulated equine chondrocyte construct. Crystals were mainly located in superficial regions of cartilage, especially in joint regions of well-developed superficial layers, more often in yearlings than in adult horses. These results indicate that intramitochondrial crystals are related to the high mechanical stress in the horse joint and potentially also to the increased metabolic activity of immature individuals.
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Publication Date: 2016-12-24 PubMed ID: 28013370PubMed Central: PMC5400799DOI: 10.1007/s00418-016-1516-6Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article describes the discovery of large crystals within the mitochondria of horse chondrocytes (cartilage cells). The study suggests that these crystals, which are shown to have high nitrogen content indicating they are protein-based, are likely tied to the mechanical stress in horse joints and possibly also to the higher metabolic activity in younger horses.

Discovery of Crystals in Horse Chondrocyte Mitochondria

  • The researchers reported for the first time the presence of giant crystals inside the mitochondria of equine chondrocytes. These structures are shown to have a granular substructure of regularly aligned tiny units, which appear dark in transmission electron microscopy (TEM) images.
  • Demonstrating the crystalline nature of these structures, different zone axes of the crystals were analyzed via Fourier transformation of lattice-resolution TEM images.
  • Elemental analysis of the crystals showed a strong presence of nitrogen, suggesting they consist mainly of protein.

Characteristics of the Crystals

  • The crystals have an regular geometric shape, with cross sections displaying up to hexagonal profiles.
  • The crystals are elongated, stretching several micrometres across the cell, with some cells housing multiple crystals, occasionally grouped within a single mitochondrion.
  • Notably, the crystals were found to be preferentially aligned along the long axis of the cells, appearing in similar orientation to the chondrocytes within the tissue.

Occurrence of the Crystals

  • Superficial regions of cartilage, particularly the joint regions of well-developed superficial layers, exhibited the crystals more frequently.
  • Notably, these crystals appeared more often in yearlings (young horses) compared to adult horses. This observation hints at a potential link between these mitochondria crystals and the higher metabolic activity in immature animals.
  • The only other instance of these crystals being identified was in cartilage repair tissue from a mechanically stimulated equine chondrocyte construct.

Implication of the Findings

  • The findings suggest that the crystals might be associated with the high mechanical stress experienced in horse joints. Their occurrence in mechanically stimulated cartilage repair tissue supports this hypothesis.
  • Further studies are required to validate these findings and to understand the role and function of these intramitochondrial crystals thoroughly.

Cite This Article

APA
Nürnberger S, Rentenberger C, Thiel K, Schädl B, Grunwald I, Ponomarev I, Marlovits S, Meyer C, Barnewitz D. (2016). Giant crystals inside mitochondria of equine chondrocytes. Histochem Cell Biol, 147(5), 635-649. https://doi.org/10.1007/s00418-016-1516-6

Publication

Histochemistry and cell biology
ISSN: 1432-119X
NlmUniqueID: 9506663
Country: Germany
Language: English
Volume: 147
Issue: 5
Pages: 635-649

Researcher Affiliations

Nürnberger, S
  • Department of Trauma Surgery, Medical University of Vienna, Waehringer Guertel 18-20, 1090, Vienna, Austria. sylvia.nuernberger@meduniwien.ac.at.
  • Ludwig Boltzmann Institute for Experimental and Clinical Traumatology, AUVA Research Center, Donaueschingenstrasse 13, 1200, Vienna, Austria. sylvia.nuernberger@meduniwien.ac.at.
  • University Clinic of Dentistry, Medical University of Vienna, Sensengasse 2a, 1090, Vienna, Austria. sylvia.nuernberger@meduniwien.ac.at.
  • Austrian Cluster for Tissue Regeneration, Vienna, Austria. sylvia.nuernberger@meduniwien.ac.at.
Rentenberger, C
  • Physics of Nanostructured Materials, Faculty of Physics, University of Vienna, Boltzmanngasse 5, 1090 Vienna, Austria.
Thiel, K
  • Department of Adhesive Bonding Technology and Surfaces, Fraunhofer Institute for Manufacturing Technology and Advanced Materials, Wiener Strasse 12, 28359 Bremen, Germany.
Schädl, B
  • Ludwig Boltzmann Institute for Experimental and Clinical Traumatology, AUVA Research Center, Donaueschingenstrasse 13, 1200, Vienna, Austria.
  • University Clinic of Dentistry, Medical University of Vienna, Sensengasse 2a, 1090, Vienna, Austria.
  • Austrian Cluster for Tissue Regeneration, Vienna, Austria.
Grunwald, I
  • Department of Adhesive Bonding Technology and Surfaces, Fraunhofer Institute for Manufacturing Technology and Advanced Materials, Wiener Strasse 12, 28359 Bremen, Germany.
Ponomarev, I
  • Research Centre for Medical Technics and Biotechnology, Geranienweg 7, 99947, Bad Langensalza, Germany.
Marlovits, St
  • Department of Trauma Surgery, Medical University of Vienna, Waehringer Guertel 18-20, 1090, Vienna, Austria.
  • Austrian Cluster for Tissue Regeneration, Vienna, Austria.
Meyer, Ch
  • Clinic and Polyclinic for Traumatology, University of Giessen, Rudolf-Buchheim-Straße 7, 35385, Giessen, Germany.
  • Orthopaedic and Trauma Surgery, Klinikum Saarbrücken, Winterberg 1, 66119, Saarbrücken, Germany.
Barnewitz, D
  • Research Centre for Medical Technics and Biotechnology, Geranienweg 7, 99947, Bad Langensalza, Germany.

MeSH Terms

  • Animals
  • Cartilage, Articular / cytology
  • Cartilage, Articular / ultrastructure
  • Chondrocytes / cytology
  • Chondrocytes / ultrastructure
  • Horses
  • Microscopy, Electron, Transmission
  • Mitochondria / chemistry
  • Mitochondria / ultrastructure
  • Stress, Mechanical

Conflict of Interest Statement

CONFLICT OF INTEREST: The authors declare that they have no conflict of interest except of the research grants mentioned in the funding section. ETHICAL APPROVAL: All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

References

This article includes 69 references
  1. Acharya KR, Ackerman SJ. Eosinophil granule proteins: form and function.. J Biol Chem 2014 Jun 20;289(25):17406-15.
    doi: 10.1074/jbc.R113.546218pmc: PMC4067173pubmed: 24802755google scholar: lookup
  2. Bancroft J, Gamble M. Theory and practice of histological techniques. 6.
  3. Banerjee A, Weidinger A, Hofer M, Steinborn R, Lindenmair A, Hennerbichler-Lugscheider S, Eibl J, Redl H, Kozlov AV, Wolbank S. Different metabolic activity in placental and reflected regions of the human amniotic membrane.. Placenta 2015 Nov;36(11):1329-32.
    doi: 10.1016/j.placenta.2015.08.015pubmed: 26386652google scholar: lookup
  4. Barastegui CA, Ruano-Gil D. Atypical cristae (paracrystalline inclusions) in mitochondria of epithelial cells of the rat ureter. I. Ultrastructural features.. J Submicrosc Cytol 1984 Apr;16(2):299-305.
    pubmed: 6325722
  5. Bechtel DB, Bulla LA Jr. Electron microscope study of sporulation and parasporal crystal formation in Bacillus thuringiensis.. J Bacteriol 1976 Sep;127(3):1472-81.
    pmc: PMC232943pubmed: 182671doi: 10.1128/jb.127.3.1472-1481.1976google scholar: lookup
  6. Bhagwat AG, Ross RC. Hepatic intramitochondrial crystalloids.. Arch Pathol 1971 Jan;91(1):70-7.
    pubmed: 5538623
  7. Brama PA, Holopainen J, van Weeren PR, Firth EC, Helminen HJ, Hyttinen MM. Effect of loading on the organization of the collagen fibril network in juvenile equine articular cartilage.. J Orthop Res 2009 Sep;27(9):1226-34.
    doi: 10.1002/jor.20866pubmed: 19242977google scholar: lookup
  8. Davis LE. Intramitochondrial crystals in Hydra.. J Ultrastruct Res 1967 Nov;21(1):125-33.
    doi: 10.1016/S0022-5320(67)80009-1pubmed: 4384439google scholar: lookup
  9. Djaldetti M, Feller N. Crystalline cytoplasmic inclusions in the liver cells of two mongrel dogs.. Res Exp Med (Berl) 1978 Sep 25;173(3):279-83.
    doi: 10.1007/BF01851499pubmed: 214832google scholar: lookup
  10. Dogan S, Barnes L, Cruz-Vetrano WP. Crystal-storing histiocytosis: report of a case, review of the literature (80 cases) and a proposed classification.. Head Neck Pathol 2012 Mar;6(1):111-20.
    doi: 10.1007/s12105-011-0326-3pmc: PMC3311947pubmed: 22430767google scholar: lookup
  11. Ericsson JL, Orrenius S, Holm I. Alterations in canine liver cells induced by protein deficiency. Ultrastructural and biochemical observations.. Exp Mol Pathol 1966 Aug;5(4):329-49.
    doi: 10.1016/0014-4800(66)90038-4pubmed: 4288293google scholar: lookup
  12. Farrants GW, Hovmöller S, Stadhouders AM. Two types of mitochondrial crystals in diseased human skeletal muscle fibers.. Muscle Nerve 1988 Jan;11(1):45-55.
    doi: 10.1002/mus.880110109pubmed: 3340100google scholar: lookup
  13. Ghadially FN, Parry EW. Ultrastructure of a human hepatocellular carcinoma and surrounding non-neoplastic liver.. Cancer 1966 Dec;19(12):1989-2004.
    doi: 10.1002/1097-0142(196612)19:12<1989::AID-CNCR2820191226>3.0.CO;2-Rpubmed: 4289039google scholar: lookup
  14. Gouranton J, Thomas D. Cytochemical, ultrastructural, and autoradiographic study of the intranuclear crystals in the midgut cells of Gyrinus marinus Gyll.. J Ultrastruct Res 1974 Aug;48(2):227-41.
    doi: 10.1016/S0022-5320(74)80079-1pubmed: 4367321google scholar: lookup
  15. Greving I, Cai M, Vollrath F, Schniepp HC. Shear-induced self-assembly of native silk proteins into fibrils studied by atomic force microscopy.. Biomacromolecules 2012 Mar 12;13(3):676-82.
    doi: 10.1021/bm201509bpubmed: 22352290google scholar: lookup
  16. Hall JD, Crane FL. Intracristal rods. A new structure in beef heart mitochondria.. J Cell Biol 1971 Feb;48(2):420-5.
    doi: 10.1083/jcb.48.2.420pmc: PMC2108177pubmed: 4101526google scholar: lookup
  17. Hamilton DW, Fawcett DW, Christensen AK. The liver of the slender salamander Batrachoseps attenuatus. I. The structure of its crystalline inclusions.. Z Zellforsch Mikrosk Anat 1966;70(3):347-63.
    doi: 10.1007/BF00336502pubmed: 5995369google scholar: lookup
  18. Hanzlíková V, Schiaffino S. Mitochondrial changes in ischemic skeletal muscle.. J Ultrastruct Res 1977 Jul;60(1):121-33.
    doi: 10.1016/S0022-5320(77)80048-8pubmed: 195077google scholar: lookup
  19. Hasegawa H, Wendling J, He F, Trilisky E, Stevenson R, Franey H, Kinderman F, Li G, Piedmonte DM, Osslund T, Shen M, Ketchem RR. In vivo crystallization of human IgG in the endoplasmic reticulum of engineered Chinese hamster ovary (CHO) cells.. J Biol Chem 2011 Jun 3;286(22):19917-31.
    doi: 10.1074/jbc.M110.204362pmc: PMC3103367pubmed: 21464137google scholar: lookup
  20. Hawkes F. Presence of a crystal in the cytoplasm of the male germ cells of the garden dormouse Eliomys quercinus L.. J Submicrosc Cytol Pathol 1993 Jul;25(3):407-15.
    pubmed: 8402541
  21. Hawkins WE, Howse HD, Foster CA. Prismatic cristae and paracrystalline inclusions in mitochondria of myocardial cells of the oyster Crassostrea virginica Gmelin.. Cell Tissue Res 1980;209(1):87-94.
    doi: 10.1007/BF00219925pubmed: 7428026google scholar: lookup
  22. Hofer F, Grogger W, Kothleitner G, Warbichler P. Quantitative analysis of EFTEM elemental distribution images. Ultramicroscopy 1997;67:83–103.
    doi: 10.1016/S0304-3991(96)00106-4google scholar: lookup
  23. Horký D, Tichý F. Ultrastructure of feline articular cartilage in the postnatal period. Acta Vet Brno 1995;64:63–70.
    doi: 10.2754/avb199564010063google scholar: lookup
  24. Horký D, Tichý F. Submicroscopic structure of equine articular cartilage. Acta Vet Brno 2002;71:151–157.
    doi: 10.2754/avb200271020151google scholar: lookup
  25. Horký D, Tichý F. Submicroscopic structure of canine articular cartilage. Vet Med Czech 2004;49:207–216.
  26. Jain M, Aiyer HM, Bajaj P, Dhar S. Intracytoplasmic and intranuclear Reinke's crystals in a testicular Leydig-cell tumor diagnosed by fine-needle aspiration cytology: a case report with review of the literature.. Diagn Cytopathol 2001 Sep;25(3):162-4.
    doi: 10.1002/dc.2029pubmed: 11536438google scholar: lookup
  27. Jones D, Bhatia VK, Krausz T, Pinkus GS. Crystal-storing histiocytosis: a disorder occurring in plasmacytic tumors expressing immunoglobulin kappa light chain.. Hum Pathol 1999 Dec;30(12):1441-8.
    doi: 10.1016/S0046-8177(99)90166-1pubmed: 10667422google scholar: lookup
  28. Kiernan JA. Histological and histochemical methods: theory and practice. 3.
  29. Klepal W, Rentenberger C, Zheden V, Adam S, Gruber D. Structural peculiarities of the penis of Semibalanus balanoides (Linnaeus, 1767) and Chthamalus stellatus (Poli, 1791) (Crustacea: Cirripedia: Thoracica). J Exp Mar Biol Ecol 2010;392:228–233.
    doi: 10.1016/j.jembe.2010.04.023google scholar: lookup
  30. Koopmann R, Cupelli K, Redecke L, Nass K, Deponte DP, White TA, Stellato F, Rehders D, Liang M, Andreasson J, Aquila A, Bajt S, Barthelmess M, Barty A, Bogan MJ, Bostedt C, Boutet S, Bozek JD, Caleman C, Coppola N, Davidsson J, Doak RB, Ekeberg T, Epp SW, Erk B, Fleckenstein H, Foucar L, Graafsma H, Gumprecht L, Hajdu J, Hampton CY, Hartmann A, Hartmann R, Hauser G, Hirsemann H, Holl P, Hunter MS, Kassemeyer S, Kirian RA, Lomb L, Maia FR, Kimmel N, Martin AV, Messerschmidt M, Reich C, Rolles D, Rudek B, Rudenko A, Schlichting I, Schulz J, Seibert MM, Shoeman RL, Sierra RG, Soltau H, Stern S, Strüder L, Timneanu N, Ullrich J, Wang X, Weidenspointner G, Weierstall U, Williams GJ, Wunderer CB, Fromme P, Spence JC, Stehle T, Chapman HN, Betzel C, Duszenko M. In vivo protein crystallization opens new routes in structural biology.. Nat Methods 2012 Jan 29;9(3):259-62.
    doi: 10.1038/nmeth.1859pmc: PMC3429599pubmed: 22286384google scholar: lookup
  31. Kozina V, Geist D, Kubinová L, Bilić E, Karnthaler HP, Waitz T, Janáček J, Chernyavskiy O, Krhen I, Ježek D. Visualization of Reinke's crystals in normal and cryptorchid testis.. Histochem Cell Biol 2011 Feb;135(2):215-28.
    doi: 10.1007/s00418-011-0782-6pubmed: 21287192google scholar: lookup
  32. Kuznetsov AV, Troppmair J, Sucher R, Hermann M, Saks V, Margreiter R. Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role?. Biochim Biophys Acta 2006 May-Jun;1757(5-6):686-91.
    doi: 10.1016/j.bbabio.2006.03.014pubmed: 16712778google scholar: lookup
  33. Lemasters JJ, Holmuhamedov E. Voltage-dependent anion channel (VDAC) as mitochondrial governator--thinking outside the box.. Biochim Biophys Acta 2006 Feb;1762(2):181-90.
    doi: 10.1016/j.bbadis.2005.10.006pubmed: 16307870google scholar: lookup
  34. Mesa H, Gilles S, Smith S, Dachel S, Larson W, Manivel JC. The mystery of the vanishing Reinke crystals.. Hum Pathol 2015 Apr;46(4):600-6.
    doi: 10.1016/j.humpath.2015.01.004pubmed: 25682153google scholar: lookup
  35. Moura EF, Ventrella MC, Motoike SY. Anatomy, histochemistry and ultrastructure of seed and somatic embryo of Acrocomia aculeata (Arecaceae). Sci Agric 2010;67:399–407.
    doi: 10.1590/S0103-90162010000400004google scholar: lookup
  36. Nagano T, Otsuki I. Reinvestigation of the fine structure of Reinke's crystal in the human testicular interstitial cell.. J Cell Biol 1971 Oct;51(1):148-61.
    doi: 10.1083/jcb.51.1.148pmc: PMC2108260pubmed: 4329518google scholar: lookup
  37. Nürnberger S, Klepal W, Vecsei V, Marlovits S. Ultrastructural insights into the world of cartilage—electron microscopy of articular cartilage. Osteosynth Trauma Care 2006;14:168–180.
    doi: 10.1055/s-2006-942270google scholar: lookup
  38. Nürnberger S, Tichy B, Jagersberger T, Vécsei V, Marlovits S. Histological aspects of articular cartilage. Osteosynth Trauma Care 2006;14:158–167.
    doi: 10.1055/s-2006-942284google scholar: lookup
  39. Nürnberger S. (Ultra-)structural details of cells and matrix during cartilage regeneration and differentiation in MACT-treated defects in the horse. J Tissue Sci Eng 2013;S2:p1–p10.
  40. Nürnberger S, Meyer C, Ponomarev I, Barnewitz D, Resinger C, Klepal W, Albrecht C, Marlovits S. Equine articular chondrocytes on MACT scaffolds for cartilage defect treatment.. Anat Histol Embryol 2013 Oct;42(5):332-43.
    doi: 10.1111/ahe.12018pubmed: 23323689google scholar: lookup
  41. O'Gorman E, Fuchs KH, Tittmann P, Gross H, Wallimann T. Crystalline mitochondrial inclusion bodies isolated from creatine depleted rat soleus muscle.. J Cell Sci 1997 Jun;110 ( Pt 12):1403-11.
    pubmed: 9217326doi: 10.1242/jcs.110.12.1403google scholar: lookup
  42. Pabst MA, Rentenberger C, Bock E, Schmied R, Lackner M, Letofsky-Papst I, Wilhelm P, Crailsheim K, Karnthaler HP. Protein crystals in the testes of the adult Apis mellifera at different ages. In: Proceedings of the 16th international microscopy Congress, p 534.
  43. Pease D. Histological techniques for electron microscopy. .
  44. Peña CE. Periodic units in the intracristal and envelope spaces of neuronal mitochondria. An artifact due to delayed fixation.. Acta Neuropathol 1980;51(3):249-50.
    doi: 10.1007/BF00687394pubmed: 6255723google scholar: lookup
  45. Pernas L, Scorrano L. Mito-Morphosis: Mitochondrial Fusion, Fission, and Cristae Remodeling as Key Mediators of Cellular Function.. Annu Rev Physiol 2016;78:505-31.
    doi: 10.1146/annurev-physiol-021115-105011pubmed: 26667075google scholar: lookup
  46. Pfanner N, Meijer M. The Tom and Tim machine.. Curr Biol 1997 Feb 1;7(2):R100-3.
    doi: 10.1016/S0960-9822(06)00048-0pubmed: 9081657google scholar: lookup
  47. Ponomarev IV, Kochneva LM, Barnewitz D. Effect of 3D chondrocyte culturing conditions on the formation of extracellular matrix in cartilage tissue-engineering constructs.. Bull Exp Biol Med 2014 Feb;156(4):548-55.
    doi: 10.1007/s10517-014-2394-3pubmed: 24771447google scholar: lookup
  48. Reinke F. Beiträge zur Histologie des Menschen. I. Über Krystalloidbildungen in den interstitiellen Zellen des menschlichen Hodens. Arch Mikr Anat 1896;47:34–44.
    doi: 10.1007/BF02975071google scholar: lookup
  49. Riopel M, Li J, Fellows GF, Goodyer CG, Wang R. Ultrastructural and immunohistochemical analysis of the 8-20 week human fetal pancreas.. Islets 2014;6(4):e982949.
    doi: 10.4161/19382014.2014.982949pmc: PMC4588500pubmed: 25425025google scholar: lookup
  50. Romeis B. Mikroskopische Technik. 17 edn.
  51. Saito A, Fleischer S. Intramitochondrial tubules in adrenal glands of rat.. J Ultrastruct Res 1971 Jun;35(5):642-9.
    doi: 10.1016/S0022-5320(71)80016-3pubmed: 4335054google scholar: lookup
  52. Santos Hde S. The ultrastructure of the mucous granules from starfish tube feet.. J Ultrastruct Res 1966 Oct;16(3):259-68.
    doi: 10.1016/S0022-5320(66)80061-8pubmed: 5929365google scholar: lookup
  53. Sawaya MR, Cascio D, Gingery M, Rodriguez J, Goldschmidt L, Colletier JP, Messerschmidt MM, Boutet S, Koglin JE, Williams GJ, Brewster AS, Nass K, Hattne J, Botha S, Doak RB, Shoeman RL, DePonte DP, Park HW, Federici BA, Sauter NK, Schlichting I, Eisenberg DS. Protein crystal structure obtained at 2.9 Å resolution from injecting bacterial cells into an X-ray free-electron laser beam.. Proc Natl Acad Sci U S A 2014 Sep 2;111(35):12769-74.
    doi: 10.1073/pnas.1413456111pmc: PMC4156696pubmed: 25136092google scholar: lookup
  54. Schönherr R, Klinge M, Rudolph JM, Fita K, Rehders D, Lübber F, Schneegans S, Majoul IV, Duszenko M, Betzel C, Brandariz-Nuñez A, Martinez-Costas J, Duden R, Redecke L. Real-time investigation of dynamic protein crystallization in living cells.. Struct Dyn 2015 Jul;2(4):041712.
    doi: 10.1063/1.4921591pmc: PMC4711630pubmed: 26798811google scholar: lookup
  55. Shiraki K, Neustein HB. Intramitochondrial crystalloids and amorphous granules. Occurrence in experimental hepatic ischemia in dogs.. Arch Pathol 1971 Jan;91(1):32-40.
    pubmed: 5538620
  56. Silvestro SR, Chapman GB. A transmission electron microscope study of "New Dawn" climber rose (Rosa wichuraiana x safrano) exhibiting rose rosette disease.. Plant Cell Rep 2004 Nov;23(5):345-51.
    doi: 10.1007/s00299-004-0838-3pubmed: 15517277google scholar: lookup
  57. Spicer S, Lillie R. Histochemical identification of basic proteins with Biebrich scarlet at alkaline pH. Stain Technol 1961;6:365–370.
    doi: 10.3109/10520296109113312google scholar: lookup
  58. Suganuma Y, Yamamoto H. Occurrence, composition, and structure of mitochondrial crystals in a hypotrichous ciliate.. J Ultrastruct Res 1980 Jan;70(1):21-36.
    doi: 10.1016/S0022-5320(80)90019-2pubmed: 6766191google scholar: lookup
  59. Swenson O, Grana L, Inouye T, Donnellan WL. Immediate and long-term effects of acute hepatic ischemia.. Arch Surg 1967 Sep;95(3):451-63.
    doi: 10.1001/archsurg.1967.01330150127017pubmed: 6035469google scholar: lookup
  60. Taira K. Studies on intramitochondrial inclusions in the pancreatic acinar cells of the Japanese newt, Triturus pyrrogaster. I. Occurrence of intramitochondrial inclusions with long-term starvation.. J Ultrastruct Res 1979 Apr;67(1):89-94.
    doi: 10.1016/S0022-5320(79)80021-0pubmed: 221664google scholar: lookup
  61. Tandler B, Hoppel CL. Studies on giant mitochondria.. Ann N Y Acad Sci 1986;488:65-81.
    doi: 10.1111/j.1749-6632.1986.tb46548.xpubmed: 3555262google scholar: lookup
  62. Thamwiriyasati N, Sakdee S, Chuankhayan P, Katzenmeier G, Chen CJ, Angsuthanasombat C. Crystallization and preliminary X-ray crystallographic analysis of a full-length active form of the Cry4Ba toxin from Bacillus thuringiensis.. Acta Crystallogr Sect F Struct Biol Cryst Commun 2010 Jun 1;66(Pt 6):721-4.
    doi: 10.1107/S1744309110015344pmc: PMC2882780pubmed: 20516610google scholar: lookup
  63. Tsutsui H, Jinno Y, Shoda K, Tomita A, Matsuda M, Yamashita E, Katayama H, Nakagawa A, Miyawaki A. A diffraction-quality protein crystal processed as an autophagic cargo.. Mol Cell 2015 Apr 2;58(1):186-93.
    doi: 10.1016/j.molcel.2015.02.007pubmed: 25773597google scholar: lookup
  64. Veenhuis M, Kiel JA, Van Der Klei IJ. Peroxisome assembly in yeast.. Microsc Res Tech 2003 Jun 1;61(2):139-50.
    doi: 10.1002/jemt.10323pubmed: 12740820google scholar: lookup
  65. Voelz H. Structural comparison between intramitochondrial and bacterial crystalloids.. J Ultrastruct Res 1968 Oct;25(1):29-36.
    doi: 10.1016/S0022-5320(68)80057-7pubmed: 4974314google scholar: lookup
  66. WARD RT. The origin of protein and fatty yolk in Rana pipiens. II. Electron microscopical and cytochemical observations of young and mature oocytes.. J Cell Biol 1962 Aug;14(2):309-41.
    doi: 10.1083/jcb.14.2.309pmc: PMC2106099pubmed: 14004944google scholar: lookup
  67. Westrate LM, Drocco JA, Martin KR, Hlavacek WS, MacKeigan JP. Mitochondrial morphological features are associated with fission and fusion events.. PLoS One 2014;9(4):e95265.
    doi: 10.1371/journal.pone.0095265pmc: PMC3986258pubmed: 24733410google scholar: lookup
  68. Whittaker P. Polarized light microscopy in biomedical research. Microsc Anal 1995;44:15–17.
  69. Ponomarev I, Wilke I. Manufacturing process for three-dimensional tissue structures und structures obtainable thereby. .

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    doi: 10.1007/s12035-022-02813-7pubmed: 35364801google scholar: lookup
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