Abstract
Hydrophobic tropoelastin molecules aggregate in vitro in physiological conditions and form fibers very similar to natural ones (Bressan, G. M., I. Pasquali Ronchetti, C. Fornieri, F. Mattioli, I. Castellani, and D. Volpin, 1986, J. Ultrastruct. Molec. Struct. Res., 94:209-216). Similar hydrophobic interactions might be operative in in vivo fibrogenesis. Data are presented suggesting that matrix glycosaminoglycans (GAGs) prevent spontaneous tropoelastin aggregation in vivo, at least up to the deamination of lysine residues on tropoelastin by matrix lysyl oxidase. Lysyl oxidase inhibitors beta-aminopropionitrile, aminoacetonitrile, semicarbazide, and isonicotinic acid hydrazide were given to newborn chicks, to chick embryos, and to newborn rats, and the ultrastructural alterations of the aortic elastic fibers were analyzed and compared with the extent of the enzyme inhibition. When inhibition was greater than 65% all chemicals induced alterations of elastic fibers in the form of lateral aggregates of elastin, which were always permeated by cytochemically and immunologically recognizable GAGs. The number and size of the abnormal elastin/GAGs aggregates were proportional to the extent of lysyl oxidase inhibition. The phenomenon was independent of the animal species. All data suggest that, upon inhibition of lysyl oxidase, matrix GAGs remain among elastin molecules during fibrogenesis by binding to positively charged amino groups on elastin. Newly synthesized and secreted tropoelastin has the highest number of free epsilon amino groups, and, therefore, the highest capability of binding to GAGs. These polyanions, by virtue of their great hydration and dispersing power, could prevent random spontaneous aggregation of hydrophobic tropoelastin in the extracellular space.
MeSH Terms
Amino Acid Oxidoreductases/metabolism
Animals
Aorta, Thoracic/cytology,metabolism,ultrastructure
Chickens
Elastin/metabolism
Glycosaminoglycans/metabolism
Kinetics
Microscopy, Electron
Protein-Lysine 6-Oxidase/metabolism
Chemicals
Glycosaminoglycans
Elastin
Amino Acid Oxidoreductases
Protein-Lysine 6-Oxidase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Fornieri C
Institute of General Pathology, University of Modena, Italy.
Baccarani-Contri M
Quaglino D
Pasquali-Ronchetti I
References (33)
33 references, click to expand
-
A defect in the intramolecular and intermolecular cross-linking of collagen caused by penicillamine. I. Metabolic and functional abnormalities in soft tissues.
J Biol Chem. 1968 Apr 10;243(7):1457-66
PMID: 5647265
-
Aortic elastin abnormalities in osteogenesis imperfecta type II.
Coll Relat Res. 1986 Dec;6(5):409-21
PMID: 3816142
-
Changes in collagen metabolism associated with the administration of penicillamine and various amino and thiol compounds.
Biochem Pharmacol. 1969 Apr;18(4):707-14
PMID: 5788514
-
The smooth muscle cell. I. In vivo synthesis of connective tissue proteins.
J Cell Biol. 1971 Jul;50(1):159-71
PMID: 4327463
-
Properties of chick tropoelastin.
Biochim Biophys Acta. 1973 Jul 12;317(1):193-201
PMID: 4723245
-
Communication: Coacervation of tropoelastin results in fiber formation.
J Biol Chem. 1974 Feb 10;249(3):997-8
PMID: 4359779
-
Catalytic activity of aortic lysyl oxidase in an insoluble enzyme-substrate complex.
Biochim Biophys Acta. 1974 Sep 13;365(1):223-34
PMID: 4472024
-
Elastin--proteoglycan interaction. Conformational changes of alpha-elastin induced by the interaction.
Connect Tissue Res. 1975;4(1):51-4
PMID: 3386
-
Simultaneous localization of proteoglycan by light and electron microscopy using toluidine blue O. A study of epiphyseal cartilage.
J Histochem Cytochem. 1976 May;24(5):621-9
PMID: 132503
-
Collagen cross-linking. Effect of D-penicillamine on cross-linking in vitro.
J Biol Chem. 1977 Jan 10;252(1):254-9
PMID: 13066
-
Elastin cross-linking in vitro. Studies on factors influencing the formation of desmosines by lysyl oxidase action on tropoelastin.
Biochem J. 1978 Sep 1;173(3):857-62
PMID: 30449
-
Lysyl oxidase.
Int Rev Connect Tissue Res. 1979;8:73-118
PMID: 41816
-
The synthesis of soluble and insoluble elastin in chicken aorta as a function of development and age. Effect of a high cholesterol diet.
Can J Biochem. 1979 Nov;57(11):1273-80
PMID: 540239
-
Immunological determinants of proteoglycans. Antibodies against the unsaturated oligosaccharide products of chondroitinase ABC-digested cartilage proteoglycans.
J Biol Chem. 1980 Aug 10;255(15):7102-5
PMID: 6156167
-
Elastin structure, biosynthesis, and relation to disease states.
N Engl J Med. 1981 Mar 5;304(10):566-79
PMID: 7005671
-
Alterations of the connective tissue components induced by beta-aminopropionitrile.
Exp Mol Pathol. 1981 Aug;35(1):42-56
PMID: 7250335
-
Interaction of a tropoelastin model with connective tissue components.
Connect Tissue Res. 1981;9(1):63-8
PMID: 6456128
-
Immunogold staining procedure for the localisation of regulatory peptides.
Peptides. 1982 May-Jun;3(3):259-72
PMID: 6181490
-
Banded fibers in tropoelastin coacervates at physiological temperatures.
J Ultrastruct Res. 1983 Mar;82(3):335-40
PMID: 6842657
-
A simple post-embedding system for the rapid demonstration of tissue antigens under the electron microscope.
Histochem J. 1983 Jun;15(6):543-55
PMID: 6409845
-
Elastin-associated microfibrils and microfibrillar proteins.
Int Rev Connect Tissue Res. 1983;10:97-209
PMID: 6358100
-
Elastin fiber-associated glycosaminoglycans in beta-aminopropionitrile-induced lathyrism.
Exp Mol Pathol. 1984 Apr;40(2):235-45
PMID: 6705893
-
Secretion of elastin in the embryonic chick aorta as visualized by immunoelectron microscopy.
Coll Relat Res. 1984 Mar;4(2):153-64
PMID: 6373117
-
Extracellular matrix-specific induction of elastogenic differentiation and maintenance of phenotypic stability in bovine ligament fibroblasts.
J Cell Biol. 1984 May;98(5):1804-12
PMID: 6725400
-
Cross-linking in collagen and elastin.
Annu Rev Biochem. 1984;53:717-48
PMID: 6148038
-
Elastin: relation of protein and gene structure to disease.
Lab Invest. 1984 Dec;51(6):605-23
PMID: 6150137
-
Elastin-proteoglycans association revealed by cytochemical methods.
Connect Tissue Res. 1985;13(3):237-49
PMID: 3159541
-
Alterations of elastin fibrogenesis by inhibition of the formation of desmosine crosslinks. Comparison between the effect of beta-aminopropionitrile (beta-APN) and penicillamine.
Connect Tissue Res. 1985;14(2):159-67
PMID: 2934220
-
The inhibition of protein-lysine 6-oxidase by various lathyrogens. Evidence for two different mechanisms.
Biochem J. 1985 Nov 15;232(1):293-6
PMID: 4084235
-
Immunohistochemical localization of chondroitin sulfate in normal and pathological human muscle.
J Neurol Sci. 1986 May;73(3):233-44
PMID: 3088212
-
Effect of DL-penicillamine on the aorta of growing chickens. Ultrastructural and biochemical studies.
Am J Pathol. 1986 Sep;124(3):436-47
PMID: 2876639
-
Relevance of aggregation properties of tropoelastin to the assembly and structure of elastic fibers.
J Ultrastruct Mol Struct Res. 1986 Mar;94(3):209-16
PMID: 3805787
-
The cross-linking of collagen and elastin: enzymatic conversion of lysine in peptide linkage to alpha-aminoadipic-delta-semialdehyde (allysine) by an extract from bone.
Proc Natl Acad Sci U S A. 1968 Oct;61(2):708-16
PMID: 5246001