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. 1984 May 1;98(5):1705–1709. doi: 10.1083/jcb.98.5.1705

Radioautographic characterization of successive compartments along the rough endoplasmic reticulum-Golgi pathway of collagen precursors in foot pad fibroblasts of [3H]proline-injected rats

PMCID: PMC2113191  PMID: 6725395

Abstract

Young rats given an intravenous injection of [3H]proline were killed at successive times from 4 to 80 min later. Fibroblasts from the front foot pad were radioautographed ; silver grains were counted over several of the organelles and the results were expressed as percent radiolabel per unit volume. These percentages reached a peak over rough endoplasmic reticulum cisternae at 4 min, intermediate vesicles and tubules at 10 min, spherical distensions of cis-side Golgi saccules at 20 min, cylindrical distensions of trans-side saccules between 40 and 60 min, and secretory granules at 60 min. It is proposed that the succession of peaks corresponds to the migration pathway of collagen precursor proteins within fibroblasts; that is, the proteins synthesized in rough endoplasmic reticulum are delivered by intermediate vesicles and/or tubules to the spherical distensions of cis-side saccules, somehow pass from there to the cylindrical distensions of trans-side saccules and, finally, are carried by secretory granules to the extracellular space.

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Selected References

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  1. Ashhurst D. E., Costin N. M. The secretion of collagen by insects: uptake of [3H]proline by collagen-synthesizing cells in Locusta migratoria and Galleria mellonella. J Cell Sci. 1976 Mar;20(2):377–403. doi: 10.1242/jcs.20.2.377. [DOI] [PubMed] [Google Scholar]
  2. Bergeron J. J., Rachubinski R. A., Sikstrom R. A., Posner B. I., Paiement J. Galactose transfer to endogenous acceptors within Golgi fractions of rat liver. J Cell Biol. 1982 Jan;92(1):139–146. doi: 10.1083/jcb.92.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bornstein P. The biosynthesis of collagen. Annu Rev Biochem. 1974;43(0):567–603. doi: 10.1146/annurev.bi.43.070174.003031. [DOI] [PubMed] [Google Scholar]
  4. Bruns R. R., Hulmes D. J., Therrien S. F., Gross J. Procollagen segment-long-spacing crystallites: their role in collagen fibrillogenesis. Proc Natl Acad Sci U S A. 1979 Jan;76(1):313–317. doi: 10.1073/pnas.76.1.313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Castle J. D., Jamieson J. D., Palade G. E. Radioautographic analysis of the secretory process in the parotid acinar cell of the rabbit. J Cell Biol. 1972 May;53(2):290–311. doi: 10.1083/jcb.53.2.290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cho M. I., Garant P. R. An electron microscopic radioautographic study of collagen secretion in periodontal ligament fibroblasts of the mouse: I. Normal fibroblasts. Anat Rec. 1981 Dec;201(4):577–586. doi: 10.1002/ar.1092010402. [DOI] [PubMed] [Google Scholar]
  7. Fessler J. H., Fessler L. I. Biosynthesis of procollagen. Annu Rev Biochem. 1978;47:129–162. doi: 10.1146/annurev.bi.47.070178.001021. [DOI] [PubMed] [Google Scholar]
  8. Griffiths G., Quinn P., Warren G. Dissection of the Golgi complex. I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus. J Cell Biol. 1983 Mar;96(3):835–850. doi: 10.1083/jcb.96.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Haddad A., Smith M. D., Herscovics A., Nadler N. J., Leblond C. P. Radioautographic study of in vivo and in vitro incorporation of fucose-3H into thyroglobulin by rat thyroid follicular cells. J Cell Biol. 1971 Jun;49(3):856–877. doi: 10.1083/jcb.49.3.856. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jamieson J. D., Palade G. E. Intracellular transport of secretory proteins in the pancreatic exocrine cell. I. Role of the peripheral elements of the Golgi complex. J Cell Biol. 1967 Aug;34(2):577–596. doi: 10.1083/jcb.34.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Karim A., Cournil I., Leblond C. P. Immunohistochemical localization of procollagens. II. Electron microscopic distribution of procollagen I antigenicity in the odontoblasts and predentin of rat incisor teeth by a direct method using peroxidase linked antibodies. J Histochem Cytochem. 1979 Jul;27(7):1070–1083. doi: 10.1177/27.7.89154. [DOI] [PubMed] [Google Scholar]
  12. Kopriwa B. A comparison of various procedures for fine grain development in electron microscopic radioautography. Histochemistry. 1975 Aug 28;44(3):201–224. doi: 10.1007/BF00491492. [DOI] [PubMed] [Google Scholar]
  13. Leblond C. P., Wright G. M. Steps in the elaboration of collagen by odontoblasts and osteoblasts. Methods Cell Biol. 1981;23:167–189. doi: 10.1016/s0091-679x(08)61498-3. [DOI] [PubMed] [Google Scholar]
  14. Marchi F., Leblond C. P. Collagen biogenesis and assembly into fibrils as shown by ultrastructural and 3H-proline radioautographic studies on the fibroblasts of the rat food pad. Am J Anat. 1983 Oct;168(2):167–197. doi: 10.1002/aja.1001680206. [DOI] [PubMed] [Google Scholar]
  15. Nadler N. J. Quantitation and resolution in electron microscope radioautography. J Histochem Cytochem. 1979 Nov;27(11):1531–1533. doi: 10.1177/27.11.512340. [DOI] [PubMed] [Google Scholar]
  16. Neutra M., Leblond C. P. Synthesis of the carbohydrate of mucus in the golgi complex as shown by electron microscope radioautography of goblet cells from rats injected with glucose-H3. J Cell Biol. 1966 Jul;30(1):119–136. doi: 10.1083/jcb.30.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Prockop D. J., Kivirikko K. I., Tuderman L., Guzman N. A. The biosynthesis of collagen and its disorders (first of two parts). N Engl J Med. 1979 Jul 5;301(1):13–23. doi: 10.1056/NEJM197907053010104. [DOI] [PubMed] [Google Scholar]
  18. Ross R., Benditt E. P. Wound healing and collagen formation. V. Quantitative electron microscope radioautographic observations of proline-H3 utilization by fibroblasts. J Cell Biol. 1965 Oct;27(1):83–106. doi: 10.1083/jcb.27.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Roth J., Berger E. G. Immunocytochemical localization of galactosyltransferase in HeLa cells: codistribution with thiamine pyrophosphatase in trans-Golgi cisternae. J Cell Biol. 1982 Apr;93(1):223–229. doi: 10.1083/jcb.93.1.223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Rothman J. E. The Golgi apparatus: roles for distinct 'cis' and 'trans' compartments. Ciba Found Symp. 1982;(92):120–137. doi: 10.1002/9780470720745.ch7. [DOI] [PubMed] [Google Scholar]
  21. Rothman J. E. The golgi apparatus: two organelles in tandem. Science. 1981 Sep 11;213(4513):1212–1219. doi: 10.1126/science.7268428. [DOI] [PubMed] [Google Scholar]
  22. Salpeter M. M., Bachmann L., Salpeter E. E. Resolution in electron microscope radioautography. J Cell Biol. 1969 Apr;41(1):1–32. doi: 10.1083/jcb.41.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Salpeter M. M. H3-proline incorporation into cartilage: electron microscope autoradiographic observations. J Morphol. 1968 Apr;124(4):387–421. doi: 10.1002/jmor.1051240402. [DOI] [PubMed] [Google Scholar]
  24. Sodek J. A comparison of the rates of synthesis and turnover of collagen and non-collagen proteins in adult rat periodontal tissues and skin using a microassay. Arch Oral Biol. 1977;22(12):655–665. doi: 10.1016/0003-9969(77)90095-4. [DOI] [PubMed] [Google Scholar]
  25. Sodek J., Brunette D. M., Feng J., Heersche J. N., Limeback H. F., Melcher A. H., Ng B. Collagen synthesis is a major component of protein synthesis in the periodontal ligament in various species. Arch Oral Biol. 1977;22(12):647–653. doi: 10.1016/0003-9969(77)90094-2. [DOI] [PubMed] [Google Scholar]
  26. Tartakoff A., Vassalli P. Plasma cell immunoglobulin M molecules. Their biosynthesis, assembly, and intracellular transport. J Cell Biol. 1979 Nov;83(2 Pt 1):284–299. doi: 10.1083/jcb.83.2.284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Trelstad R. L., Hayashi K. Tendon collagen fibrillogenesis: intracellular subassemblies and cell surface changes associated with fibril growth. Dev Biol. 1979 Aug;71(2):228–242. doi: 10.1016/0012-1606(79)90166-0. [DOI] [PubMed] [Google Scholar]
  28. Weinstock A., Leblond C. P. Elaboration of the matrix glycoprotein of enamel by the secretory ameloblasts of the rat incisor as revealed by radioautography after galactose- 3 H injection. J Cell Biol. 1971 Oct;51(1):26–51. doi: 10.1083/jcb.51.1.26. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weinstock M. Centrosymmetrical cross-banded structures in the matrix of rat incisor predentin and dentin. J Ultrastruct Res. 1977 Nov;61(2):218–229. doi: 10.1016/s0022-5320(77)80089-0. [DOI] [PubMed] [Google Scholar]
  30. Weinstock M., Leblond C. P. Synthesis, migration, and release of precursor collagen by odontoblasts as visualized by radioautography after (3H)proline administration. J Cell Biol. 1974 Jan;60(1):92–127. doi: 10.1083/jcb.60.1.92. [DOI] [PMC free article] [PubMed] [Google Scholar]

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