Rev. sci. tech. Off. int. Epiz., 1989,
8 (1), 163-176.
Physical and biochemical surface properties
of Gram-positive bacteria in relation to adhesion
to bovine mammary cells and tissues
A review of the literature
W. MAMO *
Summary: Functional properties of cell-wall components of Gram-positive
bacteria and outer cell-wall structures (such as extracellular capsule and "slime")
are reviewed in relation to pathogenicity. The possession of an extracellular
polysaccharide in the form of capsule and/or slime layer by some Gram-positive
bacteria is associated with increased virulence and resistance to phagocytosis.
Moreover, the influence of non-specific factors such as cell-surface
hydrophobicity and surface charge mediates interactions between bacteria and
host tissue cells. The role of specific interactions between bacterial adhesins
and the host epithelium in bovine mastitis is also reviewed.
KEYWORDS: Bacterial adhesion - Bovine mastitis - Collagen - Extracellular
polysaccharide capsule/slime - Fibrinogen - Fibronectin - Hydrophobicity Staphylococcus - Streptococcus - Surface charge.
INTRODUCTION
Bacterial adhesion is important in various areas of environmental, medical and
industrial research (33). Apart from the essential role of selective bacterial adhesion
in establishing many natural microbial communities, it is also crucial to such diverse
phenomena as the colonisation associated with plant and animal diseases (13, 21)
and host phagocytic defence (100). Adhesion of bacteria to animal cells, mediated
by adhesin-receptor interaction, is an initial step in the infection process. Thus,
bacterial adhesion may be exploited beneficially, e.g. to prevent pathogen colonisation
(13).
This paper reviews the literature on physical and biochemical surface properties
of Gram-positive bacteria and certain aspects of bacterial adhesion, including non­
specific macroscopic and specific molecular interactions.
* Section of Bacteriology and Epizootiology, Department of Veterinary Microbiology, College of
Veterinary Medicine, Swedish University of Agricultural Sciences, Biomedicum, Box 583, S-751 23 Uppsala,
Sweden.
164
BACTERIAL PHYSICO-CHEMICAL SURFACE PROPERTIES
A N D SURFACE STRUCTURE
Gram-positive bacteria have a relatively thick cell wall consisting mainly of
peptidoglycan (74). This is a rigid layer containing a variety of polymers, such as
teichoic and teichuronic acids (74, 107) together with polysaccharides and various
proteins, such as protein A (87), M protein (99), fibronectin (102, 81), fibrinogen
(Clumping Factor, CF) (82, 32) and collagen-binding proteins (91). Some of these
molecules are present at, and probably extend from the outer surface of the organism,
whereas others are concealed inside the cell wall. Peptidoglycan is also exposed at
the bacterial surface. Some species or strains also possess cell wall-associated polymers
in the form of capsules, or they form an extracellular slime layer (94, 16).
Hydrophobicity/hydrophilicity
The cell surface of staphylococci and streptococci has been studied for a long
time. The molecular nature of the bacterial cell surface is crucial in the interaction
between the micro-organisms and the host (71).
Bacterial hydrophobicity/hydrophilicity is a major physico-chemical property of
their surface and is associated with adhesion to host tissue cells and to inert surfaces
(93, 68, 90, 76, 23, 105, 75). Hydrophobic (water-insoluble) molecules tend to
aggregate and expel water molecules, or they may associate with water-immiscible
solvents, while hydrophilic (charged) molecules form hydrogen bonds with water and
thus associate with water molecules (98).
Factors determining staphylococcal and streptococcal cell-surface hydrophobicity
have not yet been defined. Several reports have provided evidence that certain proteins
associated with cell walls and cell membranes are responsible for bacterial cell-surface
hydrophobicity (76, 36, 42, 60, 75, 71).
The presence of M protein (105) and lipoteichoic acid (60) in the cell wall of group
A streptococci or protein A in Staph. aureus may contribute to cell-surface
hydrophobicity. Hogt et al. (37) reported that protein constituents at the cell surface
of coagulase-negative staphylococci affect hydrophobicity. Proteins sensitive to pepsin
appear to be the major hydrophobic sites at the cell-wall surface. These structures
might contribute to the non-specific adhesion of bacteria by means of hydrophobic
interaction (37, 20).
Bacterial surface hydrophobicity is dependent on growth conditions and upon
growth phase of the organism (53, 111, 71, 56). Several methods for quantifying the
hydrophobic surface properties of bacteria have been developed, including
precipitation of bacteria by salts such as ammonium sulphate (51), where highly
hydrophobic cells precipitate at low ammonium sulphate concentration; hydrophobic
interaction between non-polar regions on the bacterial cell surface (90, 52), based
on adherence to liquid hydrocarbons (76); an aqueous polymer biphasic system
consisting of solutions of dextran and polyethylene glycol (93, 60); and the association
of adherence of bacteria onto plastic surfaces with hydrophobicity (36).
Of 72 strains of Staph. aureus isolated from cases of bovine mastitis, 76% of
the strains possessed hydrophobic surface properties after in vitro cultivation on blood
agar plates (43) and hydrophobicity was correlated with protein A production. It was
165
reported recently that cultivation of Staph. aureus in a media containing bovine milk
renders the bacterial cell surface hydrophilic (57).
Bacterial surface charge
This reflects the complex chemistry of the cell surface. In Gram-positive bacteria,
teichoic and teichuronic acids of the cell wall and acidic polypeptides and
polysaccharides of the glycocalyx (capsule/slime) evidently contribute to a negative
surface charge (12). Destruction of the cell-wall ribitol teichoic acid in Staph. aureus
may reduce the surface negative charge (73). Bacterial surface charge can be estimated
simply by electrophoretic mobility of the bacteria (72), isoelectric-focusing (49) and
by using fluorescent dyes (1).
Generally, the presence of hydrophilic properties implies that charged groups are
present at the bacterial cell surface (85). Nevertheless, hydrophobic bacteria may also
have a high surface charge following exposure of hydrophobic domains (35). The
surface charge of encapsulated bacteria is generally higher than that of unencapsulated
bacteria (34) since the capsule usually consists of polysaccharides containing negativelycharged uronic acid (95).
It has been demonstrated that bacterial surface charge affects the adhesion of
bacteria to surfaces (117, 35). Furthermore, both hydrophobic and electrostatic
interactions may be involved in bacterial adhesion. However, bacteria and most
mammalian cells have a negative charge under physiological conditions, which creates
repulsive forces between the cells (41). Hydrophobic interactions might serve to
overcome the electrostatic repulsion and thereby facilitate interaction between specific
binding molecules on bacteria and host cells.
Extracellular capsule and slime
Bacterial extracellular capsule is a polysaccharide-containing component which
covers bacterial cells. In contrast, slime is an extracellular bacterial product which
dissociates from bacteria placed in a liquid medium (22).
Bacterial extracellular capsule contains abundant polysaccharides and other
polymers entrapped or bound by lectin-like interactions to the polysaccharide chains
(35). Most bacterial exopolysaccharides are polymers of more than one type of sugar
residue, and they often contain uronic acids and/or pyruvyl ketal groups which confer
a negative charge on the polymers (35). The capsule of certain bacteria contains protein
(66), polyglutamic acids (92), hyaluronic acid and polymers composed of N-acetyl
glucosamine and glucuronic acids (95).
The extracellular capsule may be:
1. rigid - sufficiently organised to exclude particles (e.g. capsule delineated by
India ink staining)
2. flexible — does not exclude particles
3. integral — under normal circumstances, intimately associated with the cell
surface
4. peripheral - whose association with the cell surface is dependent on variable
factors and which may, therefore, be partly shed into the menstruum (16). It is known
that staphylococcal cells grown at elevated temperatures in high salt concentration
will form aggregates, show irregular septation and produce capsules (38, 12).
166
F u n c t i o n a l p r o p e r t i e s o f t h e extracellular c a p s u l e a n d slime i n p a t h o g e n i c i t y
Pathogenicity, defined as damage to the host, depends on the proliferation of
the putative pathogen in a suitable niche (83) to a point where its aggressive activities
impinge on host functions. In bacterial pathogenesis, persistence is the key, because
most pathogens must persist and proliferate to produce enough toxin to be effective,
or to develop a reservoir population sufficient for tissue invasion. Bacterial persistence
usually involves adhesion as an initial step. Production of glycocalyx (capsule/slime)
inhibits clearance of bacteria by macrophages (115) and provides protection from
antibacterial agents such as surfactants and chemicals (29, 80), specific antibodies
(6), phagocytes and leukocytes (84). The possession of an extracellular capsule by
organisms of different bacterial species has been correlated with increased virulence
as compared with the unencapsulated counterparts of the same organisms (11).
Bacterial extracellular slime may interfere with phagocytosis by polymorphonuclear
leukocytes through masking of the peptidoglycans (69) and teichoic acid. These
peptidoglycans have been shown to enchance opsonisation (115, 116) and hinder
diffusion of certain antibiotics (88). Moreover, phagocytosis by macrophages as well
as by polymorphonuclear leukocytes would be physically inhibited by an aggregated
clump of staphylococci joined by a complex matrix of slime fibres (12), thus forming
microcolonies which may be important for the survival of Gram-positive bacteria.
Bacterial extracellular slime is also believed to be important in bacterial adhesion and
in establishing an infection (14). It is not yet known whether extracellular slime
functions as a glue in the initial adhesion of bacteria, or whether it is produced only
after the bacteria have adhered and have been subjected to metabolic "stress" (16).
Studies on pathogenicity of Staph. aureus in the ruminant mammary gland suggest
that capsular polysaccharides are important in impeding neutrophil-mediated
phagocytosis (108). Futhermore, inclusion of Staph. aureus capsular polysaccharides
("pseudocapsule antigens") in a vaccine results in considerable protection from
experimental staphylococcal mastitis in ewes (109).
M e t h o d s for d e m o n s t r a t i n g extracellular c a p s u l e / s l i m e
The chemistry and biosynthesis of staphylococcal capsular polymers and slime
layers have been reviewed in detail elsewhere (22, 89, 114). Several methods have
been developed to identify encapsulated bacteria. These include wet and dry India
ink staining (64); patent blue staining (77); demonstration of diffuse growth in SerumSoft-Agar (26, 67, 65); antiserum agar method (110); and electron micrography using
fluorescent antibodies (119).
BACTERIAL BIOCHEMICAL SURFACE PROPERTIES
The normal microbial colonisation of sites in the body tissues by certain bacteria
requires that the bacteria first bind to extracellular secreted constituents, cell
membranes or cell matrices (9, 104).
On the cell surface of Gram-positive organisms, proteins, lipoteichoic acid (8)
and polysaccharides are exposed, and some of these are believed to mediate cell
attachment. They also possess specific receptors for various mammalian plasma
167
proteins and, by binding large amounts of such proteins, the surface characteristics
of the bacteria can be changed considerably (61, 113, 2).
Bacterial pathogens use several mechanisms to adhere to the host tissue, usually
by binding to particular protein or other structures on the surface of the host cell.
Pathogens such as E. coli, Staph. aureus, coagulase-negative staphylococci and groups
A, B, C and G of streptococci from human and animal sources can bind to whole
eukaryotic cells, as well as to isolated extracellular matrix, and plasma proteins such
as fibronectin, laminin, collagen and fibrinogen (46, 96, 27, 97, 104, 91, 47, 106,
55, 54, 58). These binding capacities could play a role in the early stage of tissue
invasion and colonisation (106).
I n t e r a c t i o n w i t h subepithelial c o n n e c t i v e tissue c o m p o n e n t s a n d p l a s m a p r o t e i n
A number of subepithelial connective tissue components can interact specifically
with eukaryotic cells and support cell adhesion (18). They are also able to influence
cell behaviour in vitro (24). Some of these components bind cells by a reaction
involving receptors (81, 118). Interactions of fibronectin, fibrinogen and collagen
with eukaryotic cells are good examples.
Fibronectin
This is a large multifunctional adhesive glycoprotein having an apparent molecular
weight of 440,000. It is found mostly on the cell surface (79, 101, 25) and is distributed
in such a wide variety of mammalian and avian tissue and cell types that it must be
a ubiquitous structural and adhesive protein (3). Fibronectin is found in a range of
basement membrane types, and there are at least three major forms of the protein:
plasma fibronectin found in blood; cellular fibronectin (cell-surface protein) found
on the surface of cultured cells; and fibronectin found in amniotic fluid (3).
Several studies report that fibronectin functions as an adhesive protein mediating
the adhesion of bacteria to eukaryotic cells (2, 86).
Recent reports suggest that a number of bacteria, as well as tissue-invading
parasites, possess specific surface molecules which bind to fibronectin. In addition,
fibronectin mediates adherence of staphylococci to endothelial cells (103) and acts
as an opsonin for the phagocytosis of Staph. aureus by polymorphonuclear cells (17,
48, 50). Binding to Gram-positive bacteria occurs preferentially at a site located in
the amino-terminal domain of fibronectin (62) whereas the eukaryotic cell binding
site is located in the centre of the polypeptide chain (27).
Fibrinogen
This is a serum protein which induces clumping of staphylococci (40) and
streptococci (44, 45). This clumping reaction depends upon a surface protein
(fibrinogen-binding protein or clumping factor, CF) (63), which interacts with
fibrinogen fragments (fragment D), (78, 31). Fibrinogen can also bind staphylococci
and streptococci, and can mediate binding to virus-infected cell cultures (19, 82).
Whitnack and Beachey (112) have demonstrated a reduced uptake of virulent
streptococci by neutrophils in the presence of fibrinogen. However, it is not clear
why fibrinogen should bind to different eukaryotic cell receptors in the process of
linking the eukaryotic cell to staphylococci and streptococci. The role of fibrinogenbinding protein in virulence is not yet known.
168
Collagen
This protein is found in the basement membrane which underlies epithelium (104).
Collagen molecules are representatives of a large family of proteins which have a
wide range of chemical and structural features (59). Nevertheless, they appear to have
an important common function. Thus, it has been reported that collagen can bind
and aggregate certain staphylococci and streptococci from human and animal
infections (91, 104, 55, 54, 58).
BACTERIAL ADHESION
TO MAMMARY CELLS A N D TISSUE COMPONENTS
AS A POSSIBLE VIRULENCE FACTOR IN BOVINE MASTITIS
Udder pathogens like Staph. aureus, Str. agalactiae and Str. dysgalactiae, enter
the udder through the teat. After entry, factors governing the development of
infectious process and inflammation (mastitis) include the organism's adherence to
the internal epithelial surfaces (28), the number of neutrophils in the mammary
secretion, the presence of antibodies to extracellular virulence determinants and ability
of the bacteria to utilise nutrients within the udder and to multiply (4). Generally,
the development of infection and inflammation depends on the balance between the
natural defence mechanisms of the gland and the number and virulence of infective
organisms. Adhesion of pathogenic micro-organisms to living cells and tissues may
also be an important determinant of pathogenicity (89, 28, 5, 7, 15).
The adhesive properties of some udder pathogens roughly parallel their prevalence
as a cause of mastitis. For example, in most cases Staph. aureus adheres well, and
causes a chronic infection with irregular acute incidences, whereas Gram-negative
E. coli and Klebsiella sp. adhere poorly, and it is unlikely that adherence has a
significant role in the pathogenesis of mastitis due to these organisms (28). However,
these organisms often contaminate the teat orifice and are isolated from mastitis milk.
Perhaps their virulence depends on other factors and products. Early reports indicated
that Str. agalactiae, Str. dysgalactiae and Str. uberis vary in their adhesive properties
(39, 10). Staph. aureus does not always invade the tissues, and inflammation (mastitis)
may be a consequence of the organism adhering to the internal duct and sinus epithelia
(30). Frost et al. (28) studied the adherence of bacteria to epithelial cells in different
regions of the mammary gland. Adherence increased from the teat sinus to lactiferous
sinus and the large milk ducts. Adhesion offers the bacteria the advantage of a firm
attachment that can withstand the purging effect of milk flow. Adhesion mechanisms
may allow the bacteria to attach and thereafter penetrate target tissues, producing
deep-seated foci. In such cases, intra-mammary antibiotic therapy would not be
completely successful in eradicating diseases such as staphylococcal mastitis (39).
Most, but not all, of the adhesins reported so far are proteins. In general, bacteria
utilise lectin-carbohydrate interactions or non-lectin-receptor interactions. Bacteria
utilising the latter mechanisms bind to tissues through the agency of a third substance,
which attaches the bacterium to a target cell, forming a bacterium-cell complex. These
mediating (bridging) substances may be bacterial products or host-derived molecules
(15). Alternatively the bacteria may attach to a tissue surface by binding first to an
intermediary cell which in turn binds to the tissue surface. It has been reported (30)
that group B streptococci utilise the protein-mediated adhesion mechanism in bovine
udder.
169
The ability of udder pathogens to adhere specifically to host cells by means of
specific cell surface adhesins may enable infective foci to become established (70).
Moreover, antibodies against adhesion determinants of udder pathogens may prevent
the bacteria from attaching to the surface epithelium, thus being retained in the
lactating mammary gland and producing mastitis.
ACKNOWLEDGEMENTS
I wish to thank Professor Ingmar Mansson, Professor Olof Holmberg, Dr Per
Jonsson, Dr Mats Lindahl and Dr Dennis Watson for their valuable comments.
*
* *
PROPRIÉTÉS PHYSIQUES ET BIOCHIMIQUES D E L A S U R F A C E DES BACTÉRIES
GRAM-POSITIVES EN R A P P O R T A V E C L ' A D H É S I O N A U X CELLULES ET A U X
TISSUS M A M M A I R E S D E BOVINS. R E V U E B I B L I O G R A P H I Q U E . - W. M a m o .
Résumé : Les propriétés fonctionnelles des constituants de la paroi cellulaire
des bactéries Gram-positives et des structures extérieures de leur paroi cellulaire
(telles que capsule et enveloppe «visqueuse» extracellulaires) sont passées en
revue dans leur rapport avec le pouvoir pathogène. La possession, par certaines
bactéries Gram-positives, d'un polyholoside extracellulaire sous forme de capsule
et/ou de couche «visqueuse», est associée à un accroissement de leur virulence
et de leur résistance à la phagocytose. En outre, l'influence de facteurs non
spécifiques, tels que l'hydrophobicité et la charge de la surface cellulaire,
intervient dans les interactions entre les bactéries et les cellules tissulaires de
l'hôte. Le rôle des interactions spécifiques entre les facteurs d'attachement
bactériens et l'épithélium de l'hôte dans le cas de la mammite bovine est
également étudié.
MOTS-CLÉS : Adhésion bactérienne - Capsule/enveloppe visqueuse
extracellulaire polyholoside - Charge de surface - Collagène - Fibrinogène Fibronectine - Hydrophobicité - Mammite bovine - Staphylococcus Streptococcus.
*
* *
P R O P I E D A D E S FÍSICAS Y BIOQUÍMICAS D E LA SUPERFICIE D E LAS BACTERIAS
GRAM-POSITIV AS RESPECTO A LA A D H E S I Ó N A LAS CÉLULAS Y LOS TEJIDOS
MAMARIOS D E BOVINOS. REVISTA BIBLIOGRÁFICA. - W. M a m o .
Resumen: Se analizan las propiedades funcionales de los constituyentes de la
pared celular de las bacterias gram-positivas y de las estructuras exteriores de
ésta (cápsula y envoltura «viscosa» extracelulares) en su relación con la patogenicidad. La posesión, por algunas bacterias gram-positivas, de un polisacárido
extracelular en forma de cápsula y/o de capa «viscosa» va asociada con un
aumento de su virulencia y su resistencia a la fagocitosis. Además, la influencia
de factores no específicos, como la hidrofobicidad y la carga de la superficie
celular, intervienen en las interacciones entre las bacterias y las células tisulares
170
del huésped. También se analiza el papel de las interacciones específicas entre
los factores de adhesión de bacterias y el epitelio del huésped en el caso de la
mastitis bovina.
PALABRAS CLAVE: Adhesión de bacterias - Cápsula/envoltura viscosa
extracelular polisacárida - Carga de superficie - Colágeno - Estafilococo Estreptococo - Fibrinógeno - Fibronectina - Hidrofobicidad - Mastitis bovina.
*
**
REFERENCES
1. AARONSON S. (1981). - Chemical communication at the microbial level, Volume 1. CRC
Press, Boca Raton, Florida, USA.
S.N., BEACHEY E . H . & SIMPSON W.A. ( 1 9 8 3 ) . - Adherence of Streptococcus
pyogenes, Escherichia coli and Pseudomonas aeruginosa to fibronectin-coated and uncoat
epithelial cells. Infect. Immun., 4 1 , 1 2 6 1 - 1 2 6 8 .
2 . ABRAHAM
3 . AKIYAMA S.K., YAMADA K . M . & HAYASHI M. (1981). - The structure of fibronectin and
its role in cellular adhesion. J. Supramol. Struct. Cell Biochem., 1 6 , 3 4 5 - 3 5 8 .
4. ANDERSON J.C. (1976). — Mechanisms of staphylococcal virulence in relation to bovine
mastitis. Brit. vet. J., 1 3 2 , 2 2 9 - 2 4 5 .
5. ARBUTHNOTT J . P . & SMYTH S.J. (1979).
-
Bacterial adhesion in host/pathogen
interactions in animals. In Adhesion of microorganisms to surfaces. Soc. Gen. Microbiol.
Symposium. D.C. Elwood, J. Meiling & P. Rutter (eds.). Academic Press, London, 165-193.
6. BALTIMORE R.S. & MITCHELL M. (1980). - Immunologic investigation of mucoid strains
of Pseudomonas aeruginosa: comparison of susceptibility to opsonic antibody in mucoid
and non-mucoid strains. J. infect. Dis., 1 4 1 , 2 3 8 - 2 4 7 .
7. BEACHEY E . H . (1981). - Bacteria adherence: adhesin-receptor interactions mediating the
attachment of bacteria to mucosal surfaces. J. infect. Dis., 1 4 3 , 3 2 5 - 3 4 5 .
8. BEACHEY E . H . & OFEK I. (1976). - Epithelial cell binding of group A Streptococci by
lipoteichoic acid on fimbriae denuded of M protein. J. exp. Med., 1 4 3 , 7 5 9 - 7 7 1 .
9 . BJÖRK L. & KRONVALL G. (1981). - Analysis of bacterial cell wall proteins and human
serum proteins bound to bacterial cell surfaces. Acta Path. Microbiol. Scand. (B), 8 9 , 1-6.
10. BRAMLEY A.J. & HOGBEN E.M. (1982). - The adhesion of human and bovine isolates
of Streptococcus agalactiae to bovine mammary gland epithelial cells. J. comp. Path., 9 2 ,
131-137.
11. BROOK I. & WALKER R.I. (1983). - Infectivity of organisms recovered from polymicrobial
abscesses. Infect. Immun., 4 2 , 9 8 6 - 9 8 9 .
12. CAPUTY
G.G. & COSTERTON
J.W. (1982).
-
Morphological examination of the
glycocalyces of Staphylococcus aureus strains, Wiley and Smith. Infect. Immun., 3 6 ,
759-767.
13. CHENG K . J . , IRVIN R.T. & COSTERTON J.W. ( 1 9 8 7 ) . - Autochthonous and pathogenic
colonization of animal tissues by bacteria. Can. J. Microbiol., 2 7 , 4 6 1 - 4 9 0 .
14. CHRISTENSEN G.D., SIMPSON W.A., BISNO A.L. & BEACHEY E . H . (1983). -
Experimental
foreign body infections in mice challenged with slime-producing Staphylococcus epidermidi.
Infect. Immun., 4 0 , 4 0 7 - 4 1 0 .
15. CHRISTENSEN G.D., SIMPSON W.A. & BEACHEY E . H . ( 1 9 8 5 ) . - Adhesion of bacteria to
animal tissues. In Bacterial adhesion. D.C. Savage & M. Fletcher (eds.). Plenum Press,
New York, 2 7 9 - 3 0 5 .
171
16. COSTERTON J.W., IRWIN R.T. & CHENG K.J. (1981). - The bacterial glycocalyx in nature
and disease. Ann. Rev. Microbiol., 3 5 , 2 9 9 - 3 2 4 .
17. CZOP J.K., KADISH J.L. & AUSTEN F . (1981). - Augmentation of human monocytes
opsonin-independent phagocytosis by fragments of human plasma fibronectin. Proc. Natl
Acad. Sci. USA,
78, 3649-3653.
18. DAMASKY C.H., KNUDSEN K.A. & BUCK C.A. (1985). - Integral membrane glycoproteins
in cell-cell and cell-substratum adhesion. In The biology of glycoproteins. R.J. Ivatt (ed.).
Plenum Publishing Corp., New York, 1-64.
19. DAVIDSON V.E. & SANFORD B. ( 1 9 8 1 ) . - Adherence of Staphylococcus aureus to
influenza A virus infected Madin-Darby canine kidney cell cultures. Infect. Immun., 3 2 ,
118-126.
20. DAYLE R.J., NESBITT W.E. & TAYLOR K.G. ( 1 9 8 2 ) . - On the mechanism of adherence
of Streptococcus saginus to hydroxylapatite. FEMS Microbiol. Letters, 1 5 , 1-5.
21. DAZZO F.B. (1980). — Microbial adhesion to plant surfaces. In Microbial adhesion to
surfaces. R.C.W. Berkeley, J.M. Lynch, J. Meiling, P . Rutter & B. Vincent (eds.). Ellis
Horwood, Chichester, UK, 311-328.
22. DUGUID J.P. ( 1 9 5 1 ) . - The demonstration of bacterial capsules and slime. J. Path. Bact.,
63, 673-685.
2 3 . EDEBO L., KIHLSTRÖM K., MAGNUSSON E. & STENDAHL O. ( 1 9 8 0 ) . -
The hydrophobic
effect and charge effects in the adhesion of enterobacteriae to animal cell surfaces and
the influences of antibodies of different immunoglobulin classes. In Cell adhesion and
mobility. Third symposium of the British Society for Cell Biology. A.S.G. Curtis & J.D.
Pitts (eds.). Cambridge University Press, Cambridge, 65-101.
24. EKBLOM P., THESLEFF I. & SARIOLA H. (1985). -
The extracellular matrix in tissue
morphogenesis and angiogenesis. In The cell in contact. G.M. Edelman & J.P. Thiery (eds.).
John Wiley & Sons, New York, 365-394.
25. ERIKSEN M.O., CLEMMENSEN I., HANSEN M.S. & IBSEN K.K. ( 1 9 8 2 ) .
-
Plasma
fibronectin concentration in normal subjects. Scand. J. Clin. Lab. Invest., 42, 2 9 1 - 2 9 5 .
26. FINKELSTEIN R.A. & SULKIN S.E. (1958). -
Characteristics of coagulase-positive and
coagulase-negative staphylococci in serum-soft agar. J. Bact., 7 5 , 3 3 9 - 3 4 4 .
27. FRÖMAN G., SWITALSKI L.M., FARIS A., WADSTRÖM T. & HÖÖK M. ( 1 9 8 4 ) . -
Binding
of E. coli to fibronectin. A mechanism of tissue adherence. J. Biol. Chem., 2 5 9 ,
14899-14905.
28. FROST A.J., WANASINGHE D.P. & WOLLCOCK J.B. (1977). -
Some factors affecting
selective adherence of microorganisms in the bovine mammary gland. Infect. Immun., 1 5 ,
245-253.
J.R.W. ( 1 9 7 5 ) . — Mucoid strains of Pseudomonas aeruginosa. The influence of
culture medium on the stability of mucus production. J. Med. Microbiol., 8 , 5 1 3 - 5 2 2 .
30. HAGAN W.A. (1981). - The genera Staphylococcus and Streptococcus. In Hagan and
Bruner's infectious diseases of domestic animals. J.H. Gillespie & J . F . Timoney (eds.).
Cornell University Press, Ithaca, USA, 164-169.
29. GOVAN
31. HAWIGER J., TIMMONS S., COTTRELL B.A., RILEY M. & DOOLITTLE R . F . ( 1 9 8 2 ) .
-
Identification of a region of human fibrinogen interaction with staphylococcal clumping
factor. Biochemistry, 2 1 , 1 4 0 7 - 1 4 1 3 .
32. HAWIGER J., KLOCZEWIAK M. & TIMMONS S. (1983). - Interactions of fibrinogen with
staphylococcal clumping factor and with platelets. Ann. N.Y. Acad. Sci., 4 0 8 , 5 2 1 .
33. HENDRICK J.B. & WEERKAMP A.H. (1987). - Specific and non-specific interaction in
bacterial adhesion to solid substrata. FEMS Rev., 4 6 , 1 6 5 - 1 7 3 .
34. HILL M.J., JAMES A.M. & MAXTED W.R. (1963). - Some physical investigation of the
behaviour of bacterial surface. VIII. Studies on the capsular material of Streptococcus
pyogenes. Biochim. Biophys. Acta,
66, 264-274.
172
35. HOGT A.H. (1985). - Adhesion of coagulase-negative staphylococci onto biomaterials.
Thesis. Alfa Press, Enschede, The Netherlands, 25-71.
36. HOGT A . H . , DANKERT
J . , FEIJEN J. & DEVVIES
J . A . (1982).
-
Cell
surface
hydrophobicity of Staphylococcus and adhesion onto biomaterials. Antonie van
Leeuwenhoek, 48, 496-498.
37. HOGT A.H., DANKERT J. & FEIJEN J. (1983). - Encapsulation, slime production and
surface hydrophobicity of coagulase-negative staphylococci. FEMS Microbiol. Letters, 18,
211-215.
38. HURST A., HUGHES A. & PONTERFACT J. (1980). -
Mechanism of the temperature
protective effect of salts on Staphylococcus aureus. Can. J. Microbiol., 26, 511-517.
39. JAIN N.C. (1979). - Common mammary pathogens and factors in infection and mastitis.
J. Dairy Sci., 62, 128-134.
40. JELJASZEWICZ J . , SWITALSKI L.M. & ADLAM C. (1983). -
Staphylocoagulase and
clumping factor. In Staphylococci and staphylococcal infections. C.S.F. Easmon & C.
Adlam (eds.). Academic Press, London & New York, 525-557.
41. JONSSON P. (1986). — Virulence determinants of Staphylococcus aureus. Virulence studie
of alpha-toxin, coagulase, and protein A mutants and recombinants and studies of cellsurface hydrophobicity. Thesis, Swedish University of Agricultural Sciences, Uppsala,
Sweden, 8-68.
42. JONSSON P. & WADSTRÖM T. (1983). - High surface hydrophobicity of Staphylococcus
aureus as revealed by hydrophobic interaction chromatography. Curr. Microbiol., 8,
347-353.
43. JONSSON P. & WADSTRÖM T. (1984). - Cell surface hydrophobicity of Staphylococcus
aureus measured by the Salt Aggregation Test (SAT). Curr. Microbiol., 10, 203-210.
44. KANTOR F.S. (1965). - Fibrinogen precipitating by streptococcal M protein. I. Identity
of the reactants and stoichiometry of the reaction. J. exp. Med., 121, 858-859.
45. KRONVALL G . , SCHÖNBECK C. & MYHRE E. (1979). - Fibrinogen binding structures in
S hemolytic streptococci group A, C and G. Acta Pathol. Microbiol. Scand. (B), 87, 303-31
46. KUUSELA P. (1978). - Fibronectin binds to Staphylococcus aureus. Nature, 276, 718-720
47. LÄMMLER C , DE FREITAS J . C . , CHATWAL G . S . & BLOBEL H. (1985). -
Interactions of
immunoglobulin G , fibrinogen and fibronectin with Staphylococcus hyicus and
Staphylococcus intermedius. Zbl. Bakt. Hyg. A, 260, 232-237.
48. LANCER M.E. & SABA T.M. (1981). - Fibronectin as a cofactor necessary for optimal
granylocyte phagocytosis of Staphylococcus aureus. J. Reticuloendothel. Soc. 30, 14-15.
49. LANGTON R . W . , COLE J.S. & OVENN P.F. (1975). - Isoelectric focusing of bacteria,
species location within an isoelectric focusing column by surface charge. Arch. Oral Biol.,
20, 103-106.
50. LEE D . A . , HOIDAL J . R . , CLAWSON C.C., ONIE P . G . & PETERSON P . K . (1983).
-
Phagocytosis by polymorphonuclear leukocytes of Staphylococcus aureus and Pseudomona
aeruginosa adherent to plastic, agar or glass. J. Immunol. Methods, 63, 103-114.
51. LINDAHL M., FARIS A., WADSTRÖM T. & HJERTËN S. (1981). - A new test based on
"salting out" to measure relative surface hydrophobicity of bacteria cells. Biochim. Biophys.
Acta, 412, 51-61.
52. MAGNUSSON K . E . , DAVIER J . , GRUNDSTRÖM T., KIHLSTRÖM E. & NORMAKR S. (1980).
- Surface charge and hydrophobicity of Salmonella, E. coli and gonococci in relation
to their tendency to associate with animal cells. Scand. J. Infect. Dis., Suppl. 25, 135-140.
53. MALMQVIST T. (1983). — Bacterial hydrophobicity measured as partition of palmitic acid
between the two immiscible phases of cell surface and buffer. Acta Pathol. Microbiol.
Immunol. Scand. (B), 91, 69-73.
173
54. MAMO W . , FRÖMAN G. & WADSTRÖM T. (1986). - Bacterial adhesion as a virulence
factor in bovine mastitis. Possible role of cell surface hydrophobicity, capsule, fibronectin,
fibrinogen and collagen binding. In Proceedings of symposium on mastitis control and
hygienic production of milk. Espoo, Finland, June 10-12, M. Sandholm (ed.), 77-87.
55. MAMO W . , FRÖMAN G., SUNDÂS A. & WADSTRÖM T. (1987). - Binding of fibronectin,
fibrinogen and type Ii collagen to streptococci isolated from bovine mastitis. Microbiol.
Pathol., 2, 417-424.
56. MAMO W . , ROZGONYI F., BROWN A., HJERTÉN S. & WADSTRÖM T. (1987). - Cell surface
hydrophobicity and charge of Staphylococcus aureus and coagulase-negative staphylococci
from bovine mastitis. J. appl. Bad., 62, 241-249.
57. MAMO W . , ROZGONYI F., HJERTÉN S. & WADSTRÖM T. (1987). - Effect of milk on
surface properties of Staphylococcus aureus from bovine mastitis. FEMS Microbiol. Letters,
48, 195-200.
58. MAMO W . , FRÖMAN G. & WADSTRÖM T. (1988). - Interaction of subepithelial connective
tissue components with Staphylococcus aureus and coagulase-negative staphylococci from
bovine mastitis. Vet. Microbiol., 18, 163-176.
59. MILLER E.J. (1986). - Collagen: type, structures, distribution and functions. In Collagen,
chemistry, biology and biotechnology, Vol. 2. CRC Press, Boca Raton, Florida, USA.
60. MIÖRNER H. (1983). — Physicochemical surface properties of gram-positive cocci with
special reference to group A streptococci. Thesis, University of Lund.
61. MIÖRNER H., MYHRE E., BJÖRCK L. & KRONVALL G. (1980). -
Specific binding of
human albumin, fibrinogen and immunoglobulin G on the surface characteristics of bacterial
strains as revealed by partition experiments in polymer phase systems. Infect. Immun.,
29, 879-885.
62. MOSHER D . F . (1980). - Fibronectin. In Progress in hemostasis and thrombosis. Vol. 5.
Grune & Stratton, New York, 111-151.
63. MUCH H. (1908). - Über eine Vorstufe des Fimbrinfermentes in Kulture von
Staphylokokkus aureus. Biochem. Ztschr., 14, 143-155.
64. MUDD S. (1965). - Capsulation, pseudocapsulation and the somatic antigens of the
surface of Staphylococcus aureus. Ann. N.Y. Acad. Sci., 128, 45-56.
65. NORCROSS N . L . & OPDEBEEK J.P. (1983). - Encapsulation of Staphylococcus aureus
isolated from bovine mastitis milk. Vet. Microbiol., 8, 397-404.
66. ÖRSKOV I., BIRCH H., ANDERSSON A., DUGUID J . P . , STENDERUP J. & ÖRSKOV F. (1985).
- An adhesive protein capsule of Escherichia coli. Infect. Immun., 47, 191-200.
67. ORTHOMO T. & YOSHIDA K. (1978). - Encapsulation by transformation of strains of
Staphylococcus aureus determined by the serum-soft agar technique. Zbl. Bakt. Hyg. Abt.
I., 242, 436-445.
68. PERERS L., ANDÂKER L., EDEBO L., STENDAHL O . & TAGESSON C. (1977). -
Association
of some enterobacteria with the intestinal mucosa of mouse in relation to their partition
in aqueous polymer two-phase systems. Acta Pathol. Microbiol. Scand. (B), 85, 308-316.
69. PETERSON P.K., WILKINSON B.J., KIM Y., SCHMELING D . & ONIE P.G. (1978).
-
Influence of encapsulation on staphylococcal opsonization and phagocytosis by human
polymorphonuclear leukocytes. Infect. Immun., 19, 943-949.
70. PROCTOR R.A., CHRISMAN G. & MOSHER D . F . (1984).
-
Fibronectin induced
agglutination of Staphylococcus aureus correlation with invasiveness. J. Lab. Clin. Med.,
104, 455-469.
71. REIFSTECK F. & WILKINSON B.J. (1984). - Hydrophobicity/hydrophilicity of staphylo­
cocci. Abstracts of the Annual Meeting of the American Society for Microbiology, K-19,
150.
72. RICHMOND D . V . & FISCHER D . J . (1973). - The electrophoretic mobility of micro­
organisms. Adv. Microb. Physiol., 9, 1-27.
174
73. ROGERS H.J. (1979). - Adhesion of microorganism to surfaces: some general
considerations on the role of the envelope. In Adhesion of microorganisms to surfaces.
D.C. Elwood, J. Meiling & P . Rutter (eds.). Academic Press, New York, 87-100.
74. ROGERS H.J., PERKINS H.R. &WARD J.B. (1980). - Microbial cell walls and membranes.
Chapman and Hall, London.
75. ROSENBERG M. (1984). - Bacterial adherence to hydrocarbons: a useful technique for
studying cell surface-hydrophobicity. FEMS Microbiol. Letters, 22, 289-294.
76. ROSENBERG M., GUTNICK D. & ROSENBERG E. (1980). -
Adherence of bacteria to
hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS
Microbiol. Letters, 9, 29-33.
77. ROZGONYI F. & SELTMANN G . (1985). - Pathogenicity and virulence of methicillin
resistant Staphylococcus aureus. Slime layer production. Acta Microbiol. Hung., 32,
155-165.
78. RUNEHAGEN A., SCHÖNBECK C , HEDNER U., HESSEL B. & KRONVALL G . (1981).
-
Binding of fibronectin degradation products to Staphylococcus aureus and to /3-hemolytic
streptococci group A, C and G. Acta Pathol. Microbiol. Scand. (B), 89, 49-55.
79. RUOSLAHTI E., ENGVALL E. & HAYMAN E . G . (1981). - Fibronectin: current concepts
of its structure and function. Collagen Res., 1, 95-128.
80. RUSESKA I., ROBBINS J., LASHEN E.S. & COSTERTON J . W . (1982). -
Biocide testing
against corrosion - causing oilfield bacteria helps control plugging. Oil Gas J., 8, 253-264.
81. RYDEN C , RUBIN K., SPEZIALE P., HÖÖK M., LINDBERG M. & WADSTRÖM T. (1983).
- Fibronectin receptors from Staphylococcus aureus. J. Biol. Chem., 258, 3396-3401.
82. SANFORD B.A., DAVIDSON V.E. & RAMSAY M.A. (1982). -
Fibrinogen mediated
adherence of group A streptococci to influenza A virus-infected cell cultures. Infect.
Immun., 38, 513-520.
83. SAVAGE D.C. (1977). - Interaction between the host and its microbes. In Microbial
ecology of the gut. R.T.J. Clarke & T. Bauchops (eds.), Academic Press, New York,
277-310.
84. SCHWARZMANN S. & BORING J.R. (1971). - Antiphagocytic effect of slime from a mucoid
strain of Pseudomonas aeruginosa. Infect. Immun., 3 , 762-767.
85. SHERBET G.V. (1978). - Biophysical characterization of the cell surface. Academic Press,
London.
86. SIMPSON W . A . & BEACHEY E.H. (1983). - Adherence of group A streptococci to
fibronectin on oral epithelial cells. Infect. Immun., 389, 275-279.
87. SJÖQUIST J., MOVITZ J., JOHANSSON I.B. & HELM H. (1972). - Localization of protein
A in the bacteria. Eur. J. Biochem., 30, 190-194.
88. SLACK M.P.E. & NICHOLS W . W . (1981). - The penetration of antibiotics through sodium
alignate and through the exopolysaccharide of a mucoid Pseudomonas aeruginosa. Lancet,
2, 502.
89. SMITH M. (1977). - Microbial surfaces in relation to pathogenicity. Bact. Rev., 4 1 ,
475-500.
90. SMYTH C.J., JONSSON P., OLSSON E., SÖDERLIND O . , ROSENGREN J., HJERTÉN S. &
WADSTRÖM T. (1978). - Differences in hydrophobic surface characteristics of porcine
enteropathogenic Escherichia coli with or without K88 antigen as revealed by hydrophobic
interaction chromatography. Infect. Immun., 22, 462-472.
91. SPEZIALE P . , HÖÖK M. & WADSTRÖM T. (1985). -
Binding of type II collagen to
Staphylococcus aureus. In The staphylococci. J. Jeljaszewicz (ed.). Zbl. Bakt., Suppl. 14,
191-196.
92. STANIER R.Y., DOUDOROFF M. & ADELBERG E.A. (1970). - The microbial world. 3rd
ed., Prentice-Hall Inc., Engelwood Cliffs, USA, 330.
175
C. & EDEBO M. ( 1 9 7 3 ) . - Partition of Salmonella
typhimurium in a two-polymer aqueous phase system in relation to liability to phagocytosis.
Infect. Immun., 8, 3 6 - 4 1 .
9 3 . STENDAHL O . , TAGESSON
94. SUTHERLAND I.W. (1977). - Bacterial exopolysaccharides: their nature and production.
In Surface carbohydrates of the prokaryotic cell. I . W . Sutherland (ed.). Academic Press,
New York, 2 7 - 9 6 .
95. SUTHERLAND I . W . (1983). - Microbial exopolysaccharides: their role in microbial
adhesion in aqueous systems. CRC Crit. Rev. Microbiol., 10, 1 7 3 .
96. SWITALSKI L . M . , LJUNGH Ä . , RYDÉN C , RUBIN K., HÖÖK M. & WADSTRÖM T. ( 1 9 8 2 ) .
— Binding of fibronectin to the surface of group A, C and G streptococci isolated from
human infections. Eur. J. Clin. Microbiol., 1, 3 8 1 - 3 8 7 .
97. SWITALSKI L . M . , SPEZIALE P . , HÖÖK M., WADSTRÖM T. & TIMPL T. ( 1 9 8 4 ) . of Streptococcus pyogenes to laminin. J. Biol. Chem., 259, 3 7 3 4 - 3 7 3 8 .
Binding
98. TANFORD C. (1978). - The hydrophobic effect and the organization of living matter.
Science, 200, 1 0 1 2 - 1 0 1 8 .
9 9 . TYLEWSKA S.K., HJERTÉN S. & WADSTRÖM T. ( 1 9 7 9 ) . - Contribution of M protein to
the hydrophobic surface properties of Streptococcus pyogenes. FEMS Microbiol. Letters,
6, 2 4 9 - 2 5 2 .
100. VAN OSS E.J. ( 1 9 7 8 ) .
32, 19-39.
— Phagocytosis as a surface phenomenon. Ann. Rev. Microbiol.,
101. VARTIO R . & VAHERI A. (1983). - Fibronectin: chains of domains with diversified
functions. TIBS, 8, 4 4 2 - 4 4 4 .
102. VERBRUGH H.A.,
PETERSON P.K.,
SMITH D.E., NGUYEN B.Y.T., HOIDAL J . R . ,
WILKINSON B.J., VERHOEF J. & FURCHT L . T . (1981). - Human fibronectin binding to
staphylococcal surface proteins and its relative inefficiency in promoting phagocytosis
by human polymorphonuclear leukocytes, monocytes, and alveolar macrophages. Infect.
Immun., 3 3 , 8 1 1 - 8 1 9 .
103. VERCELOTTI G.M., LUSSENHOP D., PETERSON P.K., FURCHT L . T . , MCCARTHEY J.B.,
JACOB H.S. & MOLDOW C.F. (1984).
-
Bacterial adherence to fibronectin and
endothelial cells. A possible mechanism for bacterial tissue tropism. J. Lab. Clin. Med.,
103, 3 4 - 4 3 .
104. VERCELOTTI G.M., MCCARTHEY J.B., LINDHOLM P . , PETERSON P.K., JACOB H.S. &
FURCHT L.T. (1985). - Extracellular matrix proteins (fibronectin, laminin and type IV
collagen) bind and aggregate bacteria. Am. J. Pathol., 120, 1 3 - 2 1 .
105. WADSTRÖM T., HJERTÉN S., JONSSON P . & TYLEWSKA S. (1981). - Hydrophobic surface
properties of Staphylococcus aureus, Staphylococcus saprophyticus and Streptococcus
pyogenes. A comparative study. In Staphylococci and staphylococcal infections. J.
Jeljaszewicz (ed.). Zbl. Bakt., Suppl. 1 0 . Gustav Fischer Verlag, Stuttgart, 4 4 1 - 4 4 7 .
106. WADSTRÖM T., SWITALSKI L . M . , SPEZIALE P., RUBIN K., RYDÉN C , FRÖMAN G., FARIS
A., LINDBERG M. & HÖÖK M. (1985). - Binding of microbial pathogens to connective
tissue fibronectin: an early step in localized and invasive infections. In The pathogenesis
of bacterial infections. Springer Verlag, Berlin, Heidelberg, 193-207.
107. WARD J.B. (1981). - Teichoic and teichuronic acid: biosynthesis, assembly and location.
Microbiol. Rev., 45, 2 1 1 - 2 4 3 .
108. WATSON D.L. ( 1 9 8 2 ) . - Virulence
Res. vet. Sci., 3 2 , 3 1 1 - 3 1 5 .
of Staphylococcus aureus grown in vitro and in vivo.
109. WATSON D . L . (1988). - Vaccination against experimental staphylococcal mastitis in
ewes. Res. vet. Sci. (in press).
T.E. & APICELLA M.A. ( 1 9 8 4 ) . - Detection of encapsulations in Staphylococcus
aureus by use of antiserum agar. J. Clin. Microbiol., 20, 1 4 1 - 1 4 4 .
110. WEST
176
111. WESTERGREN C . & OLSSON J. (1983).
-
Hydrophobicity and adherence of oral
streptococci after repeated subculture in vitro. Infect. Immun., 40, 4 3 2 - 4 3 5 .
112. WHITNACK E. & BEACHEY E.H. (1982). - Antiopsonic activity of fibrinogen bound to
M protein on the surface of group A streptococci. J. Clin. Invest., 69, 1042.
A.J. & KNOX K . W . ( 1 9 8 0 ) . - Bacterial cell surface amphiphiles. Biochim.
Biophys. Acta, 604, 1-26.
114. WILKINSON B.J. (1983). - Staphylococcal capsules and slime. In Staphylococci and
staphylococcal infections. C.S.F. Easmon & C . Adlam (eds.). Academic Press, London,
Vol. 2 , 4 8 1 .
113. WICKEN
115. WILKINSON B.J., KIM Y . , PETERSON P . K . , OVIE P.G. & MICHAEL A.F. ( 1 9 7 8 ) .
-
Activation of complement by cell surface components of Staphylococcus aureus. Infect.
Immun., 20, 3 8 8 - 3 9 2 .
116. WILKINSON B.J., KIM Y . & PETERSON P.K. (1981). - Factors affecting complement
activation by Staphylococcus aureus cell walls, their components and mutants altered in
teichoic acid. Infect. Immun., 32, 2 1 6 - 2 2 4 .
117. WOOD J.M. (1980). — The interaction of microorganisms with ion exchange resin. In
Microbial adhesion to surfaces. R.C.W. Berkeley, J.M. Lynch, J. Meiling, P . Rutter &
B. Vincent (eds.). Ellis Horwood, Chichester, U K , 163-165.
118. YAMADA K . M . , AKIYAMA S.M., HASEGAWA T., HUMPHRIES M.J., KENNEDY D . W . ,
NAGATA K . , URUSHIHARA H., OLDEN K . & CHEN W . T . ( 1 9 8 5 ) . - Recent advances in
research on fibronectin and other cell-attachment proteins. J. Cell Biochem., 28, 7 9 - 9 7 .
119. YOSHIDA K . , TAKARASHI M., OTHOMO T., MINEGISHI Y . , IEHIMAN Y . & HAGA K.
(1979). — Application of fluorescent antibody for detecting capsular substances in
Staphylococcus aureus. J. appl. Bact., 46, 1 4 7 - 1 5 2 .