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. 1982 Jun 1;93(3):910–920. doi: 10.1083/jcb.93.3.910

Mammalian eyes and associated tissues contain molecules that are immunologically related to cartilage proteoglycan and link protein

PMCID: PMC2112134  PMID: 7119004

Abstract

Monospecific antibodies to bovine nasal cartilage proteoglycan monomer and link protein were used to demonstrate that immunologically related molecules are present in the bovine eye and associated tissues. With immunofluorescence microscopy, reactions for both proteoglycan and link protein were observed in the sclera, the anterior uveal tract, and the endoneurium of the optic nerve of the central nervous system. Antibody to bovine nasal cartilage proteoglycan also reacted with some connective tissue sheaths of rectus muscle and the perineurium of the optic nerve of the central nervous system. Antibody to proteoglycan purified from rat brain cross-reacted with bovine nasal cartilage proteoglycan, indicating structural similarities between these proteoglycans. ELISA studies and crossed immunoelectrophoresis demonstrated that purified dermatan sulphate proteoglycans isolated from bovine sclera did not react with these antibodies but that the antibody to cartilage proteoglycan reacted with other molecules extracted from sclera. Two molecular species resembling bovine nasal link protein in size and reactivity with antibody were also demonstrated in scleral extracts: the larger molecule was more common. Antibody to link protein reacted with the media of arterial vessels demonstrating the localization of arterial link protein described earlier. Tissues that were unstained for either molecule included the connective tissue stroma of the iris, retina, vitreous body, cornea, and the remainder of the uveal tract. These observations clearly demonstrate that tissues other than cartilage contain molecules that are immunologically related to cartilage-derived proteoglycans and link proteins.

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Selected References

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  1. Anderson H. C., Griner S. A. Cartilage induction in vitro. Ultrastructural studies. Dev Biol. 1977 Oct 15;60(2):351–358. doi: 10.1016/0012-1606(77)90133-6. [DOI] [PubMed] [Google Scholar]
  2. Axelsson I., Heinegård D. Characterization of the keratan sulphate proteoglycans from bovine corneal stroma. Biochem J. 1978 Mar 1;169(3):517–530. doi: 10.1042/bj1690517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Axelsson I., Heinegård D. Fractionation of proteoglycans from bovine corneal stroma. Biochem J. 1975 Mar;145(3):491–500. doi: 10.1042/bj1450491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benya P. D., Padilla S. R., Nimni M. E. Independent regulation of collagen types by chondrocytes during the loss of differentiated function in culture. Cell. 1978 Dec;15(4):1313–1321. doi: 10.1016/0092-8674(78)90056-9. [DOI] [PubMed] [Google Scholar]
  5. Caputo C. B., MacCallum D. K., Kimura J. H., Schrode J., Hascall V. C. Characterization of fragments produced by clostripain digestion of proteoglycans from the Swarm rat chondrosarcoma. Arch Biochem Biophys. 1980 Oct 1;204(1):220–233. doi: 10.1016/0003-9861(80)90027-2. [DOI] [PubMed] [Google Scholar]
  6. Caterson B., Baker J. R., Levitt D., Paslay J. W. Radioimmunoassay of the link proteins associated with bovine nasal cartilage proteoglycan. J Biol Chem. 1979 Oct 10;254(19):9369–9372. [PubMed] [Google Scholar]
  7. Champion B. R., Poole A. R. Immunity to homologous cartilage proteoglycans in rabbits with chronic inflammatory arthritis. Coll Relat Res. 1981 Sep;1(5):453–473. doi: 10.1016/s0174-173x(81)80029-5. [DOI] [PubMed] [Google Scholar]
  8. Christner J. E., Caterson B., Baker J. R. Immunological determinants of proteoglycans. Antibodies against the unsaturated oligosaccharide products of chondroitinase ABC-digested cartilage proteoglycans. J Biol Chem. 1980 Aug 10;255(15):7102–7105. [PubMed] [Google Scholar]
  9. Conrad G. W., Kelly P. T., von der Mark K., Edelhauser H. F. A comparative study of elasmobranch corneal and scleral collagens. Exp Eye Res. 1981 Jun;32(6):659–672. doi: 10.1016/0014-4835(81)90015-4. [DOI] [PubMed] [Google Scholar]
  10. Cöster L., Fransson L. A. Isolation and characterization of dermatan sulphate proteoglycans from bovine sclera. Biochem J. 1981 Jan 1;193(1):143–153. doi: 10.1042/bj1930143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. De Luca S., Lohmander L. S., Nilsson B., Hascall V. C., Caplan A. I. Proteoglycans from chick limb bud chondrocyte cultures. Keratan sulfate and oligosaccharides which contain mannose and sialic acid. J Biol Chem. 1980 Jul 10;255(13):6077–6083. [PubMed] [Google Scholar]
  12. Delpech B., Halavent C. Characterization and purification from human brain of a hyaluronic acid-binding glycoprotein, hyaluronectin. J Neurochem. 1981 Mar;36(3):855–859. doi: 10.1111/j.1471-4159.1981.tb01672.x. [DOI] [PubMed] [Google Scholar]
  13. Dolan D. L., Lemmon G. B., Jr, Teitelbaum S. L. Relapsing polychondritis. Analytical literature review and studies on pathogenesis. Am J Med. 1966 Aug;41(2):285–299. doi: 10.1016/0002-9343(66)90023-4. [DOI] [PubMed] [Google Scholar]
  14. Faltz L. L., Caputo C. B., Kimura J. H., Schrode J., Hascall V. C. Structure of the complex between hyaluronic acid, the hyaluronic acid-binding region, and the link protein of proteoglycan aggregates from the swarm rat chondrosarcoma. J Biol Chem. 1979 Feb 25;254(4):1381–1387. [PubMed] [Google Scholar]
  15. Gardell S., Baker J., Caterson B., Heinegård D., Rodén L. Link protein and a hyaluronic acid-binding region as components of aorta proteoglycan. Biochem Biophys Res Commun. 1980 Aug 29;95(4):1823–1831. doi: 10.1016/s0006-291x(80)80111-2. [DOI] [PubMed] [Google Scholar]
  16. Glant T., Csongor J., Szücs T. Immunopathologic role of proteoglycan antigens in rheumatoid joint disease. Scand J Immunol. 1980;11(3):247–252. doi: 10.1111/j.1365-3083.1980.tb00232.x. [DOI] [PubMed] [Google Scholar]
  17. Hardingham T. E., Muir H. The specific interaction of hyaluronic acid with cartillage proteoglycans. Biochim Biophys Acta. 1972 Sep 15;279(2):401–405. doi: 10.1016/0304-4165(72)90160-2. [DOI] [PubMed] [Google Scholar]
  18. Hardingham T. E. The role of link-protein in the structure of cartilage proteoglycan aggregates. Biochem J. 1979 Jan 1;177(1):237–247. doi: 10.1042/bj1770237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hascall V. C., Heinegård D. Aggregation of cartilage proteoglycans. I. The role of hyaluronic acid. J Biol Chem. 1974 Jul 10;249(13):4232–4241. [PubMed] [Google Scholar]
  20. Hascall V. C., Heinegård D. Aggregation of cartilage proteoglycans. II. Oligosaccharide competitors of the proteoglycan-hyaluronic acid interaction. J Biol Chem. 1974 Jul 10;249(13):4242–4249. [PubMed] [Google Scholar]
  21. Hassell J. R., Newsome D. A., Hascall V. C. Characterization and biosynthesis of proteoglycans of corneal stroma from rhesus monkey. J Biol Chem. 1979 Dec 25;254(24):12346–12354. [PubMed] [Google Scholar]
  22. Hassell J. R., Robey P. G., Barrach H. J., Wilczek J., Rennard S. I., Martin G. R. Isolation of a heparan sulfate-containing proteoglycan from basement membrane. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4494–4498. doi: 10.1073/pnas.77.8.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Heinegård D., Axelsson I. Distribution of keratan sulfate in cartilage proteoglycans. J Biol Chem. 1977 Mar 25;252(6):1971–1979. [PubMed] [Google Scholar]
  24. Heinegård D., Hascall V. C. Aggregation of cartilage proteoglycans. 3. Characteristics of the proteins isolated from trypsin digests of aggregates. J Biol Chem. 1974 Jul 10;249(13):4250–4256. [PubMed] [Google Scholar]
  25. Herman J. H., Dennis M. V. Immunopathologic studies in relapsing polychondritis. J Clin Invest. 1973 Mar;52(3):549–558. doi: 10.1172/JCI107215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Herman J. H., Wiltse D. W., Dennis M. V. Immunopathologic significance of cartilage antigenic components in rheumatoid arthritis. Arthritis Rheum. 1973 May-Jun;16(3):287–297. doi: 10.1002/art.1780160302. [DOI] [PubMed] [Google Scholar]
  27. Jenkins R. B., Hall T., Dorfman A. Chondroitin 6-sulfate oligosaccharides as immunological determinants of chick proteoglycans. J Biol Chem. 1981 Aug 25;256(16):8279–8282. [PubMed] [Google Scholar]
  28. Kiang W. L., Margolis R. U., Margolis R. K. Fractionation and properties of a chondroitin sulfate proteoglycan and the soluble glycoproteins of brain. J Biol Chem. 1981 Oct 25;256(20):10529–10537. [PubMed] [Google Scholar]
  29. Kimura J. H., Hardingham T. E., Hascall V. C., Solursh M. Biosynthesis of proteoglycans and their assembly into aggregates in cultures of chondrocytes from the Swarm rat chondrosarcoma. J Biol Chem. 1979 Apr 25;254(8):2600–2609. [PubMed] [Google Scholar]
  30. King J., Laemmli U. K. Polypeptides of the tail fibres of bacteriophage T4. J Mol Biol. 1971 Dec 28;62(3):465–477. doi: 10.1016/0022-2836(71)90148-3. [DOI] [PubMed] [Google Scholar]
  31. Linsenmayer T. F., Little C. D. Embryonic neural retina collagen: in vitro synthesis of high molecular weight forms of type II plus a new genetic type. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3235–3239. doi: 10.1073/pnas.75.7.3235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lohmander L. S., De Luca S., Nilsson B., Hascall V. C., Caputo C. B., Kimura J. H., Heinegard D. Oligosaccharides on proteoglycans from the swarm rat chondrosarcoma. J Biol Chem. 1980 Jul 10;255(13):6084–6091. [PubMed] [Google Scholar]
  33. Margolis R. U., Lalley K., Kiang W. L., Crockett C., Margolis R. K. Isolation and properties of a soluble chondroitin sulfate proteoglycan from brain. Biochem Biophys Res Commun. 1976 Dec 20;73(4):1018–1024. doi: 10.1016/0006-291x(76)90224-2. [DOI] [PubMed] [Google Scholar]
  34. Mayne R., Vail M. S., Mayne P. M., Miller E. J. Changes in type of collagen synthesized as clones of chick chondrocytes grow and eventually lose division capacity. Proc Natl Acad Sci U S A. 1976 May;73(5):1674–1678. doi: 10.1073/pnas.73.5.1674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. McKay D. A., Watson P. G., Lyne A. J. Relapsing polychondritis and eye disease. Br J Ophthalmol. 1974 Jun;58(6):600–605. doi: 10.1136/bjo.58.6.600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McMurtrey J., Radhakrishnamurthy B., Dalferes E. R., Jr, Berenson G. S., Gregory J. D. Isolation of proteoglycan-hyaluronate complexes from bovine aorta. J Biol Chem. 1979 Mar 10;254(5):1621–1626. [PubMed] [Google Scholar]
  37. Norling B., Glimelius B., Westermark B., Wasteson A. A chondroitin sulphate proteoglycan from human cultured glial cells aggregates with hyaluronic acid. Biochem Biophys Res Commun. 1978 Oct 30;84(4):914–921. doi: 10.1016/0006-291x(78)91670-4. [DOI] [PubMed] [Google Scholar]
  38. Oegema T. R., Jr, Brown M., Dziewiatkowski D. D. The link protein in proteoglycan aggregates from the Swarm rat chondrosarcoma. J Biol Chem. 1977 Sep 25;252(18):6470–6477. [PubMed] [Google Scholar]
  39. Oegema T. R., Jr, Hascall V. C., Eisenstein R. Characterization of bovine aorta proteoglycan extracted with guanidine hydrochloride in the presence of protease inhibitors. J Biol Chem. 1979 Feb 25;254(4):1312–1318. [PubMed] [Google Scholar]
  40. Pal S., Tang L. H., Choi H., Habermann E., Rosenberg L., Roughley P., Poole A. R. Structural changes during development in bovine fetal epiphyseal cartilage. Coll Relat Res. 1981 Feb;1(2):151–176. doi: 10.1016/s0174-173x(81)80017-9. [DOI] [PubMed] [Google Scholar]
  41. Poole A. R., Pidoux I., Reiner A., Tang L. H., Choi H., Rosenberg L. Localization of proteoglycan monomer and link protein in the matrix of bovine articular cartilage: An immunohistochemical study. J Histochem Cytochem. 1980 Jul;28(7):621–635. doi: 10.1177/28.7.6156200. [DOI] [PubMed] [Google Scholar]
  42. Poole A. R., Pidoux I., Rosenberg L. Role of proteoglycans in endochondral ossification: immunofluorescent localization of link protein and proteoglycan monomer in bovine fetal epiphyseal growth plate. J Cell Biol. 1982 Feb;92(2):249–260. doi: 10.1083/jcb.92.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Poole A. R., Reddi A. H., Rosenberg L. C. Persistence of Cartilage proteoglycan and link protein during matrix-induced endochondral bone development: an immunofluorescent study. Dev Biol. 1982 Feb;89(2):532–539. doi: 10.1016/0012-1606(82)90343-8. [DOI] [PubMed] [Google Scholar]
  44. Poole A. R., Reiner A., Tang L. H., Rosenberg L. Proteoglycans from bovine nasal cartilage. Immunochemical studies of link protein. J Biol Chem. 1980 Oct 10;255(19):9295–9305. [PubMed] [Google Scholar]
  45. Rajapakse D. A., Bywaters E. G. Cell-mediated immunity to cartilage proteoglycan in relapsing polychondritis. Clin Exp Immunol. 1974 Mar;16(3):497–502. [PMC free article] [PubMed] [Google Scholar]
  46. Rosenberg L., Hellmann W., Kleinschmidt A. K. Electron microscopic studies of proteoglycan aggregates from bovine articular cartilage. J Biol Chem. 1975 Mar 10;250(5):1877–1883. [PubMed] [Google Scholar]
  47. Sahu S., Lynn W. S. Isolation and characterization of proteoglycans from porcine lungs. J Biol Chem. 1979 May 25;254(10):4262–4266. [PubMed] [Google Scholar]
  48. Schmut O. The organization of tissues of the eye by different collagen types. Albrecht Von Graefes Arch Klin Exp Ophthalmol. 1978 Aug 16;207(3):189–199. doi: 10.1007/BF00411053. [DOI] [PubMed] [Google Scholar]
  49. Swann D. A., Sotman S. S. The chemical composition of bovine vitreous-humour collagen fibres. Biochem J. 1980 Mar 1;185(3):545–554. doi: 10.1042/bj1850545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tang L. H., Rosenberg L., Reiner A., Poole A. R. Proteoglycans from bovine nasal cartilage. Properties of a soluble form of link protein. J Biol Chem. 1979 Oct 25;254(20):10523–10531. [PubMed] [Google Scholar]
  51. Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Vertel B. M., Dorfman A. An immunohistochemical study of extracellular matrix formation during chondrogenesis. Dev Biol. 1978 Jan;62(1):1–12. doi: 10.1016/0012-1606(78)90088-x. [DOI] [PubMed] [Google Scholar]
  53. Vijayagopal P., Radhakrishnamurthy B., Srinivasan S. R., Berenson G. S. Studies of biologic properties of proteoglycans from bovine aorta. Lab Invest. 1980 Feb;42(2):190–196. [PubMed] [Google Scholar]
  54. Watson P. G., Hayreh S. S. Scleritis and episcleritis. Br J Ophthalmol. 1976 Mar;60(3):163–191. doi: 10.1136/bjo.60.3.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Wiebkin O. W., Bartold P. M., Thonard J. C. Proteoglycans from adult human gingival epithelium. Biochem J. 1979 Nov 1;183(2):467–470. doi: 10.1042/bj1830467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Yanagishita M., Rodbard D., Hascall V. C. Isolation and characterization of proteoglycans from porcine ovarian follicular fluid. J Biol Chem. 1979 Feb 10;254(3):911–920. [PubMed] [Google Scholar]
  57. von der Mark K., von der Mark H., Timpl R., Trelstad R. L. Immunofluorescent localization of collagen types I, II, and III in the embryonic chick eye. Dev Biol. 1977 Aug;59(1):75–85. doi: 10.1016/0012-1606(77)90241-x. [DOI] [PubMed] [Google Scholar]

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