ULTRASTRUCTURAL, PROTEIN COMPOSITION, AND ANTIGENIC COMPARISON OF PSITTACINE BEAK AND FEATHER DISEASE VIRUS PURIFIED FROM FOUR GENERA OF PSITTACINE BIRDS Author(s): Branson W. Ritchie, Frank D. Niagro, Kenneth S. Latimer, Phil D. Lukert, Walstine L. Steffens, III, Pauline M. Rakich, and Nancy Pritchard Source: Journal of Wildlife Diseases, 26(2):196-203. Published By: Wildlife Disease Association DOI: http://dx.doi.org/10.7589/0090-3558-26.2.196 URL: http://www.bioone.org/doi/full/10.7589/0090-3558-26.2.196

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of Wildlife

Journal

Diseases,

26(2),

Ic Wildlife

ULTRASTRUCTURAL, COMPARISON

PROTEIN

COMPOSITION,

OF PSITTACINE

VIRUS

PURIFIED

Branson Walstine

W. Ritchie, L. Steffens,

FROM

BEAK

FOUR

AND

GENERA

AND

1990,

Disease

pp.

196-203

Association

1990

ANTIGENIC

FEATHER

DISEASE

OF PSITTACINE

BIRDS

Frank D. Niagro,2 Kenneth S. Latimer,3 Phil D. Lukert,2 lII, Pauline M. Rakich,3 and Nancy Pntchard2

Department of Small Animal Medicine, University of Georgia, Athens, Georgia 2 Department of Medical Microbiology, University of Georgia, Athens, Georgia Department of Pathology, College of University of Georgia, Athens, Georgia Department of Anatomy and Radiology, University of Georgia, Athens, Georgia

College of Veterinary Medicine, 30602, USA College of Veterinary Medicine, 30602, USA Veterinary Medicine, 30602, USA College of Veterinary Medicine, 30602, USA

Psittacine beak and feather disease (PBFD) virus, was purified from diseased tissues of a lesser sulphur-crested cockatoo (Cacatua suiphurea), a black palm cockatoo (Probosiger aterrimus), a red-bred Amazon parrot (Amazona autumnalis), and a peach-faced lovebird (Agapornis roseicollis). The histopathology of diseased feathers and follicular epithelium from the different species was compared; basophilic intranuclear inclusion bodies were identified in the follicular epithelium and intracytoplasmic globular inclusions were observed within macrophages located in the feather pulp from the four species. Psittacine beak and feather disease virus antigen was specifically detected by colloidal gold immunoelectron microscopy. The different preparations of purified virions displayed an icosahedral symmetry, were non-enveloped, and had a mean diameter that varied from 12 to 15 nm when negatively stained. Two major viral-associated proteins with approximate molecular weights of 26 and 23 kilodaltons (kd) were consistently ABSTRACT:

demonstrated

the

from

related.

genically

diseased

birds

four

These

viral

findings

is similar

based

Purified

preparations.

that

suggest

virions

the

PBFD virus characteristics,

on ultrastructural

from purified protein

the four genera from numerous composition

were antigenera of and

antigenic

reactivity.

Key

words:

antigenic

Psittacine

similarities,

and

beak

virus

feather

disease

characterization,

INTRODUCTION

In

the

last

several

decades,

virus,

Diminuviridae,

experimental

psittacine

beak and feather disease (PBFD) has been diagnosed increasingly in a variety of psittacine birds based on clinical and histologic lesions. The syndrome generally is

ultrastructure,

(Ritchie gested

et the

family similar

to which nonpathogenic

covirus, Ritchie While

proteins,

study.

al., 1989a, b). We name Diminuviridae

may

the

belong

PBFD virus,

have virus porcine

(Tischer

et a!., 1989b). the host range

sugthe

for

of the

and

a cir-

et al.,

1982;

PBFD

virus

characterized by relatively symmetric feather dystrophy and loss, development of beak deformities and eventual death. A 14 to 16 nm icosahedral, non-enveloped virion with a single stranded circular DNA

remains largely unknown, histologic or clinically suggestive lesions of the disease have been described in the following species: sulphur-crested cockatoo (Caca-

genome of approximately bases can be consistently

tua galerita) leadbeateri),

birds with PBFD Gross and histologic PBFD have been tally by exposing

(Ritchie lesions reproduced neonatal

1.7 to 2.0 kilorecovered from et al., 1989a). consistent with experimenpsittacine birds

corella

hollandicus), glossus (Platycercus icterotis),

purified

mallee

PBFD

virions 196

Major galah

Mitchell’s cockatoo (C. roseicapilla),

sanguinea),

(C. tenuirostris), tacus undulatus),

to feather follicle homogenates containing suspected PBFD viral particles (Wylie and Pass, 1987), as well as by inoculation with concentrated

(C.

,

long-billed budgerigar cockatiel

(C. little corella

(Melopsit(Nymphicus

rainbow lorikeet (Trichohaematodus), eastern rosella eximius), western rosella (P. hooded parrot (P. dissimilis), ring-neck

parrot

(Barnardius

bar-

RITCHIE

nardi),

red-rump

haetnatonotus), zonarius),

grass Port

Bourke’s

ET AL-COMPARISON

parrot

(Psephotus

Lincoln parrot

parrot (Neophema

(B.

bourkii), Eclectus parrot (Eclectus roratus), princess parrot (Polytelis alexandrae), peach-faced lovebird (Agapornis roseicollis), nyassa lovebird (A. lilianae), Fisher’s lovebird (A. fischeri), masked lovebird (Alisterus 1984a,

personata) and king parrot scapularis) (Pass and Perry, b; Perry and Pass, 1985; Harrison,

1986).

Other

merous PBFD

additional including:

reports

have species Moluccan

phurea), Philippine (C. haematuropygia), galerita triton), rinocristata), 1984;

et

copsis

a!.,

vasa)

ease has populations

red-vented cockatoo triton cockatoo (C. citron cockatoo (C. cmcockatoo

little

atoo

and

(C.

Lowenstein,

documented of psittacine

sulphur

ahs,

(C. alba), (C. sul-

goffini),

1984;

Jacob-

in several wild birds in Australia

crested

corellas,

Major

rainbow

(CoraThe dis-

cockatoos,

gal-

Mitchell’s

lorikeets

cock-

(McOrist

et

al.,

1984; Perry and Pass, 1985). There is undocumented discussion of endemic PBFD in populations of Moluccan cockatoos, Philippine red-vented cockatoos, umbrella cockatoos While

and many

cockatoos

are

budgerigars. species

of susceptible vious

of white

included

in the

birds,

there

documentation

of

and

pink

reported

has

been

PBFD

list

beak

to be Pacific 1984b;

in

and

reported

restricted to Old psittacine species Huff et al., 1988).

feather in birds

disease within

any

of

World and (Pass and Psittacine

has the

only order

been Psitta-

ciformes. Diagnosis quired

the

of

PBFD

identification

197

and Huff

shortly (McOrist, Jacobson this

was

after emerging 1984; Pass et a!., 1986;

study,

purified

recovered

rot (Amazona faced lovebird. compared acteristics,

palm cockatoo (Probosa red-bred Amazon par-

based protein

munological

vi-

a sulphur-crested

autumnalis), and Viral preparations on

ultrastructural composition,

homology

generated against The pathology

the Perry, et a!.,

concentrated

from

cockatoo, a black iger aterrimus),

from

and

with

PBFD associated

a peachwere charim-

antibodies

virus in rabbits. with diseased

feather follicles from these birds was compared both at the light and at the electron microscopic level for reactivity of intracytoplasmic inclusion specific antibody. This to firmly ical and covery refine based tural tion,

establish histologic

from various the characteristics

bodies with viral study was designed

the association lesions with psittacine of the

of clinvirion respecies, to PBFD virus

on the commonality of ultrastrucfeatures and viral protein composito establish the presence of common

antigenic determinants among viruses purified from different diseased birds and to document the expanding host range of the PBFD virus.

no pre-

the black cockatoo genera. Prior to a recent report which described histologic lesions consistent with PBFD in a blue-fronted Amazon parrot (Arnazona aestiva), a new world Psittaciforme, the disease was thought South Perry,

VIRUS

growing follicle 1984a; 1988). In

nu-

DISEASE

inclusion epithelium of necrotic, that stop

rus

may develop cockatoo (C.

1986); and vasa parrot (Cooper et al., 1987).

been

including

that

cockatoo cockatoo

goffin

(Harrison,

shown

BEAK AND FEATHER

tracytoplasmic or intranuclear bodies in feathers or follicubar from birds with clinical signs dystrophic, nonviable feathers

(A.

moluccensis), umbrella lesser sulphur-crested

son

OF PSITTACINE

previously of basophilic

has

rein-

MATERIALS

AND METHODS

Experimental samples were collected from birds presented to the teaching hospital at the University of Georgia College of Veterinary Medicine (Athens, Georgia 30602, USA). Skin biopsies containing affected feathers were obtained from a sulphur-crested cockatoo, a black palm cockatoo, a red-bored Amazon parrot, and a peach-faced lovebird and preserved in 10% neutral buffered formabin solution. Formabinfixed tissues were processed routinely, embedded in paraffin, sectioned at 4 sm, and stained with hematoxylin and eosin. The induced pathologic changes were compared microscopically. Skin biopsies for immunoelectron microscopy were fixed, processed routinely, and embedded

198

JOURNAL

L.

ill

R.

OF WILDLIFE

VOL. 26, NO. 2, APRIL

resin

Pennsylvania,

tions grids

(Vectastain

ABC

Kit,

Vector

Laboratories,

lingame, California inhibit nonspecific tions were incubated of purified rabbit and 25 kibodalton

94010, USA) background overnight in IgG prepared proteins of the

Primary

binding

antibody

belled

with

a

1:20

of

IgG

conjugated

with

10

ticles

(Janssen

Life

Sciences

Chester, tions

nm

Pennsylvania, were

and lead electron Massachusetts Feather

follicle

cockatoo,

a

Amazon

parrot,

agnosed minced

and

viously

(Ritchie

sec-

acetate

a sulphur-crested a

a peach-faced

al.,

red-bred

lovebird

PBFD stored

performed et

The

uranyl

cockatoo,

with and

was

parWest

USA).

from

palm

clinically with scissors,

purification

gold

Products

were at as

1989a).

di-

excised,

C. Virus

-70

described Virus

pre-

suspension

(10 Ll) from each bird was mixed with 1 jl of tobacco mosaic virus (1 mg/mb Cedric Kuhn, Department of Plant Pathology, University of Georgia, Athens, Georgia 30602, USA). The virus suspension was adsorbed onto 0.25% formvar-coated grids for 5 mm, negatively stained with 1% phosphotungstic acid, and examined at 80 kV (Jeol JEM-100S). Samples of purified virus were suspended in sample buffer composed of 62.5 mM Tris-HCL, pH 6.8, 2% sodium dodecyl sulfate (SDS), 10% glycerol,

0.5%

bromphenol ples were

blue and then heated

loaded

onto

2-mercaptoethanol,

14%

0.008%

0.001% phenol red. Sam(35 C) for 5 mm, and

SDS-polyacrylamide

1 acrylamide-acrylaide

gels

cross-linker

products

Rockland,

Laemmli

buffer

Maine

04841,

Bio-

USA)),

in

a

1970). Electrophoresis was conducted at 20 ma for 3 hr. Proteins were visualized by silver staining (BioRad Laboratories Richmond, California 94804, USA). Molecular weights were determined from densitometer with

system

(40:

(FMC

tracings

a

DU-64

Instruments, USA). The

viral-associated

Virus cockatoo

of photographic

Beckman

(Beckman nia 92631,

(Laemmli,

ie et al.,

1989a),

virus-specific

were

white

rabbit

tion,

Tennessee

as previously and (Myrtels 37179,

used

An

adult

Rabbitry, USA)

of the

compared.

(Ritchanti-PBFD

New Thompson

was

sl (402 with

ng total 200

protein)

sl of Freund’s

complete adjuvant (Sigma Chemical Company, St. Louis, Missouri 63178, USA). Booster inoculations of purified virus and adjuvant were given 2 and 4 wk later. Blood was collected 1 wk after the last booster injection and rabbit IgG was purified from serum by ammonium sulfate precipitation (Hudson and Hay, 1980). The purified IgG was stored at -70 C. 26

and

23

kd

viral

associated

proteins

were separated using a 14% SDS-polyacrylamide gel as described above. The area of the gel containing these proteins was sliced out of the gel, diced, mixed with 1.5 ml of sterile water for injection and administered intramuscularly to a New Zealand White Rabbit (Myrtels Rabbitry). Booster inoculations were performed at 2 and 4 wk. IgG was purified as described above. Immunologic detection of viral antigen was performed by spotting purified virus suspensions onto nitrocel!ubose filters (0.45 sm pore size, Bio-Rad Laboratories). Filters were blocked overnight at 4 C using 2% bovine serum albumin (BSA, Sigma Chemical Company) and then blocked for 30 mm at room temperature with biotin (2Oug/ml, Sigma Chemical Company) and normal goat serum (1% Vector Laboratories, Burlingame, California 94010, USA). Filters were washed repeatedly with tween-20 tris buffered saline (TTBS) and incubated in a 1:400 dilution of rabbit anti-PBFD antibody (in 0.1% Tween 20, 1% BSA, TTBS) for 30 mm. Filters were washed repeatedly with TTBS and incubated in biotmnylated goat anti-rabbit IgG (Zymed Laboratories, Inc., McGaw Park, Illinois 60085, USA). Filters were washed repeatedly with tris buffered saline (TBS) and incubated in streptavidinabkaline phosphatase (Zymed Laboratories, Inc.) for 20 mm. Filters were washed with TBS then veronal buffer (0.15 M, pH 9). Filters were developed with 5 bromo-4

chboromndoxyl phosphate and razolium substrates according procedures (Blake et al., serum (Vector Laboratories) of rabbit anti-PBFD virus control.

nitro blue tetto established

1984). Normal rabbit was used in place antibody as a negative

RESULTS Califor-

of a Moluccan and rate zon-

described to generate

200

mixed

negatives

Inc., Fullerton, molecular weights

polypeptides

antibodies.

with virus

spectrophotometer

recovered from the skin was purified by isopycnic

al centrifugation

purified

The

Ia-

examined by transmission (Jeol JEM-100S Peabody, USA) at 80 kV.

tracts

black

was

colloidal

with

citrate and microscopy 01960,

Bur-

goat-anti-rabbit

19380,

counterstained

of

was applied to staining. Seca 1:10 dilution against the 23 PBFD virus.

subsequently

dilution

1990

tramuscularly

(Polysciences, Inc., War18976, USA). Thin secwere placed on high-transmission nickel and a 1:10 dilution of normal goat serum

rington,

White

DISEASES,

inoculated

Zealand Stain-

Feather

lesions

from

a sulphur-crested

cockatoo, a black palm cockatoo, a redbored Amazon parrot and a peach-faced lovebird diagnosed clinically with PBFD were identical (Fig. 1). Feathers occasionally appeared clubbed, constricted, misshapen follicles

or otherwise deformed. and or sheath epithelium

Feather were

RCHIE

ET AL-COMPARISON

OF PSITTACINE

BEAK AND FEATHER

DISEASE

VIRUS

199

p S

4 #{149}1

::

a ...‘

.

$1,

.*

Oil

,

$3

#{149}1

S

.* .

t

..,

;: 1.

FIGURE

a red-bred

Photomicrograph

Amazon

feather

disease.

bodies

are

pulp

(arrow).

of skin

parrot

with

Globular

present

=

macrophages

from

beak

intracytoplasmic

within

Bar

biopsy

psittacine

and

in

inclusion

the feather

Viral

10 Mm.

by necrosis

ithelial cells, and occasional

of individual

ent were macrophages sophilic, mntracytoplasmic, sion bodies (Fig. 1). observed frequently feather

with

multiple, globular These cells

of mononuclear of variable severity.

Ultrastructurally,

ithelial

cells. In was noted Also presbaincluwere

often in the feather pulp and less within the epithelium. The pulp occasionally was necrotic with

infiltration philic cells cells

inclusion

and

macrophages

viral particles arranged arrays. Colloidal gold

and

are

gold

arranged

in

labelling

antigenic

staining

proteins.

Bar

=

of

100

paracrystalline

(dark 23

dots)

arrays.

indicate

and 26 kilodalton

specific PBFD

viral

nm.

ep-

intra-and intercellular edema intranuclear basophilic in-

clusion bodies within epithelial rare instances, vesicle formation within the folbicular epithelium.

Electron micrograph of macrophage a peach-faced lovebird with PBFD.

particles

Colloidal

characterized

2. from

FIGURE

inclusion

hetero-

the gen

presence of specific PBFD within the inclusions (Fig. Ultrastructural analysis of

viral

anti-

2). negatively

stained viral preparations from each bird revealed a highly concentrated, homogenous population of 12 to 15 nm diameter, icosahedral, nonenveboped virus particles (Fig. 3). Virtually all of the virions observed negative particles

in

the stain. were

preparations Consequently, observed

with

excluded few electron

the viral dense

cores. bodies

in ep-

appeared

in paracrystalline binding indicated

as

SDS-polyacrylamide revealed that the all four the same

gel protein

viral preparations (Fig. 4). The

ebectrophoresis compositions

were molecular

virtually weights

of

200

JOURNAL

OF WILDLIFE

DISEASES,

VOL. 26, NO. 2, APRIL

j.....

1990

.. /r

-

#{248}i;/

....

.-,.

.

.

.

.

.

3.

FIGURE black

palm

graphed nm.

Electron cockatoo.

at

80

kV.

micrograph Virus

of

psittacine

suspensions

Tobacco

mosaic

and relative concentrations associated proteins (VP)

were virus

beak

(arrow:

15

of the viraldetermined

were

for each isolate by analyzing densitometer tracings of gel electrophorograms (Fig. 5). Comparison of the apparent molecular weights of the major viral proteins (VP1, 26,000;

VP2,

23,000;

and

VP3,

15,000

and

58,000

also

most of the purified As an additional edness of these viral anti-PBFD

virus

cockatoo >

.

CD CD

60

VIRUS

201

C4)

>

* **

‘I.,

A

29

vP1 VP2 0

N.

w

vP3

14.2 $1:

4.

FIGURE

Silver

electrophoresis teins

of

isolated

from

Lane

3 (red-bored

palm Lane

cockatoo) 1 bovine

bonic

anhydrase

(14,200

stained

purified Lane

SDS-polyacrylamide PBFD viral associated

2 (sulphur-crested

Amazon

cockatoo),

parrot),

Lane

and Lane 5 (peach-faced serum albumin (60,000 (29,000

daltons)

were

daltons) used

as

gel pro-

0

Cl) CD 4

4 (black lovebird).

daltons),

and

car-

@-lactalbumin

molecular

weight

stan-

dards.

C acteristics

of

trated

from

virus

purified

diseased

and

tissues

of

crested cockatoo, a black a red-bored Amazon parrot faced lovebird phology was viral birds

preparations. reported

revealed similar for The in this

palm and

that each

concena sulphur-

cockatoo, a peach0

the virus morof the purified

viruses study

purified from were also ub-

.1

.3

.2

.4

.5

.6

.7

.8

.9

1

R 5. Identification of the major viral proPhotographic negatives of electrophoretically separated viral proteins were scanned densitometricabby at 470 nm for determination of their relative FIGURE

teins.

trastructurally

covered (Ritchie

similar

to

from other et ab., 1989a).

PBFD

virus

cockatoo While there

re-

species is a slight

difference in size between the virions in this study (12 to 15 nm) and the size previously reported for PBFD virus (14 to 16 nm), these differences are considered in-

concentrations

Tracing

and

apparent

A is of viral

proteins

cockatoo.

Tracing

faced

lovebird.

black

palm

from

B is of viral Tracing

cockatoo.

a red-bored

molecular

from

proteins

C is of viral Tracing

Amazon

weights.

a sulphur-crested

D

is

from

a peach-

proteins of

from

viral

proteins

parrot.

significant. By comparing (as determined

by

the protein SDS-PAGE

munobbot detection virus purified from atoo,

a black

palm

Amazon parrot and bird, it was determined

composition and dot

im-

of viral antigens) of a sulphur-crested cockcockatoo,

a red-bored

a peach-faced that

the

lovemajor

viral

associated

species in the range

proteins

were 48,000 from

from

each

similar. Minor protein and 58,000 molecular some virab isolates are

to those obtained from ed cockatoos, umbrella

of

these

bands weight similar

other sulphur-crestcockatoos and

Mo-

a

202

JOURNAL

TABLE

1.

viral

OF WILDLIFE

Molecular

proteins

DISEASES,

weights

from

(in

various

VOL. 26, NO. 2, APRIL

daltons)

psittacine

Sulfurcrested

Black palm

cockatoo

VP1

of

PBFD

cockatoo

26,300

25,600

25,700

25,000

\P2

23,200

22,600

22,600

22,300

VP3

15,400

15,700

15,700

APP

58,700

58,600

AP2’

51,700

‘APi.

AP2

represent

molecular

minor

FIGURE ship

58,600

58,000

48,800

49,100 proteins

Lane

weights.

buccan When

cockatoos the molecular

proteins

(VP1,

VP2

they approximate of 60,000. One larger proteins tively though proteins during

(Ritchie weights and

et

al., of the

VP3)

are

1989a). smaller

summed,

a total molecular might speculate could represent

weight that these alterna-

processed translation products, alit is possible that they are host cell which become viral associated virus maturation. Partial proteo-

lytic

sequencing

teins

and

of

analysis

products

will

relationship

be of

viral of

associated

in

vitro

pro-

translation

required

to

various

viral

the

clarify

the

associated

proteins. Using to

rabbit

compare

tween

anti-PBFD the

the

four

determined

viral

that

virus

antigenic

the

viruses

each of these birds bated. The ultrastructural

antibody

similarities

be-

preparations, were

it was

recovered

from

antigenically

re-

characteristics,

of

pro-

PBFD

4

2

of

virus

psittacine

azon),

at higher

Demonstration

7.

between

era

-

viral-associated

3

2

...s Peachfaced lovebird

-

I

birds.

Red-bred Amazon parrot

Protein

1990

birds.

composition,

ties

of

Lane

Lane

lovebird

from same

each viral

lished lated

that the novel and characterized

be

consistently

psittacine Presently,

a

sulphur-

palm and

that

cockatoo, a peach-

virus

genera It is now

obtained

belong clearly

to the estab-

virus previously as PBFD virus

recovered

from

species displaying no other viral

consistently fected birds niques. This

Am-

similari-

from

suggest of these family.

(red-bored

3

antigenic

isolated

faced

gen-

cockatoo),

lovebird).

and

viruses

relationdifferent

1 (umbrella

crested cockatoo, a black a red-bored Amazon parrot

isocan

various

PBFD lesions. agent has been

purified from utilizing the investigation

follicles of indescribed techalso represents

the first reported case of PBFD in a species of black cockatoo. Although histologic lesions of PBFD have been reported for numerous species of lovebirds and a bluefronted Amazon parrot, this is the first report of PBFD virus recovery from these two

genera. At the

bevel

of analysis

investigations,

there

described is limited

in these or

genic diversity detectable with rus recovered from numerous infected psittacine birds. With species

of birds

currently

ceptible to the PBFD homology that can tween purified virus could be significant an effective PBFD

12345

from

(black palm cockatoo), and Lane 4 (peach-faced

tein

antigenic

purified

no

anti-

PBFD vispecies of the many

considered

sus-

virus, the antigenic be demonstrated befrom different genera in the development of viral vaccine.

ACKNOWLEDGMENTS 6.

FIGURE

PBFD

virus

was

titrated in protein),

(0.67

rsg

and

Lane

immunoblot an

against

described total

Dot from

total

umbrella rabbit

material

and

Lane

2 (1.3

protein),

5 (no antigen).

Lane

detection cockatoo.

of purified Viral

anti-PBFD methods: ng

total

4 (0.13

virus Lane

protein), ng total

antigen

lgG

as ng Lane 3 protein),

1 (6.7

The dividuals

financial,

John

authors and

wish

material

Vaughn,

to

thank

organizations

Grayce

and

the for

following their

professional

Ohashi,

Greg

in-

unselfish

assistance:

and

Linda

Harrison, Jane and Wade Stowe, Terry Cbyne, Smokey Mountain Caged Bird Club, Bird Clubs of Virginia, Society of Parrot Breeders and Ex-

RITCHIE

hibitors, Association

Kircher, Dawe,

American Federation of Avian Veterinarians, Mary B. Ard, M. Kathy Dick Davis, and Zeigler

LITERATURE

AND

tive

method

for

B.

H.

1987.

HARRISON,

1984.

clinics

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