A pericentric inversion of chromosome 4 in pigs

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A pericentric inversion of chromosome 4 in pigs

A Ducos, A Pinton, A Séguéla, Hm Berland, Mf Blanc, A Darré, P Pinton, M

Yerle, R Darré

To cite this version:

Original

article

A

_pericentric

inversion

of

chromosome

4

in

_pigs

A

Ducos

1

A

Pinton

A

_Séguéla

HM

Berland

MF

Blanc

A Darré

2

P

Pinton

M

Yerle

R Darré

1

Ura

Inra-ENVT de

_{cytogénétique}

des

populations animales,

École

nationale

_{vétérinaire,}

23, chemin des

_Capelles,

31076 Toulouse

_cedex;

2

École

nationale de

_formation

agronomique, Service de

_zootechnie,

31326 Castanet-Tolosan

_cedex;

3

Laboratoire de

_{génétique cellulaire,}

Institut national de la recherche

_agronomique,

Auzeville BP 27, 31326 Castanet-Tolosan

cedex,

.France

(Received

11 December

_{1996; accepted}

16

_May

₁₉₉₇₎

Summary - The main French

_porcine

artificial insemination centre

_recently

decided to carry out a

_systematic

chromosomal evaluation of the animals used for

pure-breeding

purposes. This

practice

has allowed the identification of a new

_pericentric

inversion

affecting

chromosome

4,

in four

Large

White boars

originating

from four different herds. The

cytogenetic

evaluation

by

means of the

_{GTG-banding technique}

revealed an inversion

of the

_pericentric

_part of the

_chromosome,

after double

_breaks,

the first one in the

_4q2.3

pale

band of the

_long

arm, and the second one in the _upper border of the

_4pl.4

dark band

of the short arm. The chromosomal _{rearrangement} could be

described, according

to the

standard

nomenclature,

as

38,XY,inv(4)(p14q23).

This

interpretation

has been confirmed

by

in situ

hybridization

of the cosmid BHT12 located on the

_4pl.5

band. This chromosomal

abnormality

has no

significant

effect on

production

or

reproductive performance

of carrier

animal. A rather old and common

_origin

of the

abnormality

is

hypothesized.

chromosome aberration

_/

pericentric inversion

_{/ pig /}

reproductive performance

/

FISH

Résumé - Inversion _{péricentrique du chromosome 4 chez le porc.} Le

_principal

centre

français

d’insémination

artificielle

porcine a récemment décidé de

procéder

à un contrôle

chromosomique systématique

de tous les verrats de races _pures. Cette

_pratique

a _permis de

mettre en

_évidence,

chez _quatre verrats

_Large

White issus de _quatre

_élevages

de sélection

différents,

une nouvelle inversion

_{péricentrique impliquant}

le chromosome 4. L’examen des chromosomes colorés en bandes GTG a révélé une double _cassure, la

_première

au

niveau de la bande claire

_4q2.3

du bras

_long,

la seconde en limite

_supérieure

de la

bande sombre

_l,pl.4

sur le bras _court, suivie d’une inversion de la partie

péricentrique

du chromosome. Cette anomalie peut être

décrite,

conformément

à la nomenclature en

vigueur, de

la façon

suivante :

_{38,XY,inv(4){p14q23).}

Cette

interprétation

a été

confirmée

anomalie

chromosomique

n’a pas

d’effet significatif sur

les

performances

de

production

ou

de

reproduction

des individus _porteurs. Une

_origine

commune et relativement ancienne est

envisagée.

anomalie _{chromosomique}

_/

inversion _{péricentrique}

_/

porc

/

performances de

repro-duction

_/

FISH

INTRODUCTION

Peri- or

_paracentric

inversions are chromosomal abnormalities

relatively frequent

and

_particularly

well known in humans. Individuals

_heterozygous

for the inversion

can

_produce

unbalanced

_gametes

_{(duplications,}

_deletions)

_leading

to non-viable

embryos

(hence

to a lower

fertility

of the

carriers)

or to more or less marked

phenotypic

modifications of the viable

_embryos

with an unbalanced

_karyotype:

facial

_alterations,

mental

_retardation;

see for

_example

Madan

₍₁₉₉₅₎

and Villa et al

(1995).

Such abnormalities have also been described in other animals but much less

frequently.

The first cases of

_pericentric

inversion in cattle were

_reported

as

_early

as the late sixties

(Short

et

_al,

_1969).

In most

_situations,

the identified inversions

were associated with an

_important

loss of

fertility

(Popescu,

_{1972, 1976;}

Roldan

et

al, 1984; Switonski, 1987;

Guo and

_Chen,

_1989).

In the

_{porcine species,}

the first

case of an inversion was

_{reported quite recently}

(Switonski,

1991):

a

_paracentric

inversion of chromosome 8. Since

_then,

two different

_{pericentric inversions,}

both

affecting

chromosome

_1,

have been observed

_(Miyake

et

_{al, 1994; Danielak-Czech,}

1996).

In both _cases, the inversion seemed to have no effect on the

_fertility

of

the

_carriers,

nor were

_phenotypic

abnormalities detected in the carriers or in their

offspring.

In contrast to

_inversions,

_reciprocal

translocations are

_relatively

_frequent

in the

pig.

Until now, more than 60 cases have been described

_(Ducos

et

_al,

_1997).

Those translocations

_generally

have a

large

effect on

fertility.

For this _reason, the main French

_porcine

artificial insemination centre

_recently

decided to _carry out a

_systematic

chromosomal evaluation of the animals used for

pure-breeding

purposes

(about

200

analyses

per

year).

This

practice

has allowed the identification of boars

_carrying

a new

_pericentric

inversion

_affecting

chromosome 4. The

_origin,

the distribution and the zootechnical effects of this chromosomal

abnormality

are

presented

and discussed.

MATERIAL AND METHODS Animals

The first carriers of the inversion were

purebred

Large

White boars

([1]

and

[2]

in

fig

1)

originating

from two different selection herds.

_Samples

of blood

_and/or

skin

biopsies

were taken from two

_generations

of

_offspring

of boar

_!1!,

as well as on the

Chromosomal

_study

The mitotic chromosomes were obtained from classical

synchronized

cultures

of

_lymphocytes

and fibroblasts. Chromosome

preparations

were

_spread

on cold

wet slides and air dried. Slides were treated with

0.1%

_trypsin

(Difco)

and

stained with

3%

Giemsa solution to

_generate

_GTG-banding

_{(Seabright, 1971).}

The FPG

technique previously

described for humans

_(Dutrillaux

and

_Couturier,

_1981):

BrdU

_{incorporation}

_during

the last 7

_h,

was carried out to obtain

_RBG-banding

patterns.

Chromosomes were

arranged according

to the standardized

karyotype

of

the domestic

_pig

_(Committee

for the Standardized

Karyotype

of the Domestic

_Pig,

1988).

A fluorescent in situ

_{hybridization}

was also

performed

in order to confirm the

results obtained with classical

cytogenetic

methods. The

procedure applied

has

previously

been described

by

Yerle et al

_(1994).

The GTG-banded chromosomes

were

_hybridized

with cosmid BHT12

(Hoyheim

et

_al,

₁₉₉₄₎

located on the

4pl.5

band. The chromosomes were counter-stained with

_propidium

iodide,

examined

under a Zeiss

Axiophot

_microscope,

and then

photographed

with a

Fuji

400 film.

Zootechnical

_study

Production

_performance

_(age

at 100

_kg,

backfat thickness at 100

_kg)

and

reproductive performance

(total

number of

_piglets

_born)

of the animals

_appearing

in

_figure

1

_(numbered

_animals)

have been recorded within the national

_performance

testing

programme set up in France for

genetic

evaluation purposes

(Ducos

et

_al,

1994).

Analyses

of variance were

_performed

in order to _compare

_performance

of carrier and non-carrier animals. Production

performance

data were

_analysed

_using

a linear model

_including

the fixed effects of the batch

_(a

batch was defined within each

herd as a _group of at least 15 animals of the same sex born within a 2-week

period

of time and tested at the same

time)

and of the inversion

(normal

or inverted chromosome

_4).

The

_{reproductive performance}

of boars was also

_{analysed using}

a linear model

_including

the

following

fixed effects: inversion

(normal

or inverted

chromosome

_4),

boar nested within

_inversion,

herd x _year x season x

_type

of fertilization combination

_{(contemporary}

_group)

and

_parity

number. Performance

of all sows sired

_by

boars that were carriers of the

inversion,

and

performance

of

contemporary

sows sired

by

normal boars were considered.

The effects of the inversion carried in a

homozygous

state could not be tested

statistically

owing

to the _very low number of

_homozygous

animals

_(only

two

_sows).

RESULTS

Chromosomal

study

All the

_metaphases

obtained

_(from

_lymphocytes

or

_fibroblasts)

for the first two

boars

_[1]

and

_[2]

_presented

a

_peculiar

_appearance of chromosome 4. The structure

of the other chromosomes was normal

_{(fig 2).}

On the short arm of the abnormal chromosome

_4,

the presence of two dark bands in addition to the thin dark band in

4p1.2

was observed. We also observed the

_{disappearance}

of the

_4q2.4

dark band at

was not modified. Double

_breaks,

the first one in the

_{4q2.3 pale}

band of the

_long

arm, and the second one in the _upper border of the

_4p1.4

dark band of the short

arm, followed

by

an inversion of the

pericentric

part

of the chromosome were

hypothesized

(fig 3).

The chromosomal

_{rearrangement}

could be

_described,

_according

to the standard

_{nomenclature,}

as

38,XY,inv(4)(p14q23).

The same

_abnormality

was

observed

_again

in the dam of boar

_!2!,

as well as in boars

[3]

and

!4!.

The

karyotypes

of 17

_offspring

of boar

_!1!,

_{produced by}

_mating

this boar to three different

_dams,

were

prepared.

All six

offspring

of the first dam

((9!

in

fig

1)

carried the

abnormality.

Two of them

_(females

_[5]

and

_[6]

in

_fig

₁₎

were

_homozygous

for the inversion. Three

piglets

out of

five,

and one out of

_{six, produced}

_by

females

_[16]

and

_!17!,

respectively,

carried the inversion

_(not

all the

_piglets

born in the litters shown in

_fig

1 could be

karyotyped

for reasons

_beyond

our

_control).

The

_homozygous

sow

[5]

was mated and

_produced

two successive litters. All six

_piglets

born in the first litter carried the

inversion. The second _pregnancy was not finalized

_(abortion),

for unknown reasons.

Zootechnical

_study

Production

performance

of the inversion carriers controlled on the farm or in the

station are indicated in table I. The

_performance

of ten carriers out of

_13,

and 12 carriers out of

_13,

_{respectively,}

are

_slightly

better than the _average

_performance

of

their

_{contemporaries}

_(age

at 100

_kg

and backfat thickness at 100

_kg).

_However,

the differences between carrier and non-carrier animals were not

_{statistically significant.}

The number of litters

_{produced by}

each of the four boars

_([1]

to

_[4]

in

_fig

_1),

and the _average size of these litters are

_reported

in table II. The boar

[1]

_produced

a rather

_large

number of litters. The _average litter size sired

_by

this male was

slightly higher

(+

0.8

_piglets)

than the average size of the litters

produced

by

the

other boars

_during

the same

period

in the same herds.

However,

the effect of the

inversion on

_{reproductive performance}

of boars was not

_{statistically}

_significant.

The

fertility

records of sow-carriers are

_given

in table III. The successive litters of the

sows

_heterozygous

for the inversion

(sows

[8]

and

[9]

in

fig

1)

had a normal size

(more

than ten

_piglets).

The sow

(6!,

_homozygous

for the

_inversion,

could not be fertilized after three successive

_cycles

of artificial insemination. The breeder stated that it was sterile and

_{proposed culling.}

Sow

!5!,

also

_homozygous,

had a first litter of six

_piglets,

one of them

_presenting

serious malformations

(animal

[7]

in

_fig

1).

The second

_gestation

of this sow was confirmed but was not finalized.

DISCUSSION

Among

livestock

animals,

the

porcine species

is

_probably

the one in which the

greatest

number of structural chromosomal abnormalities have been identified. The

_reciprocal

translocations have been and still are

_{intensively investigated}

owing

to their deleterious effect on

prolificacy,

the

_major

_component

of the current

French selection

_objective

_{(Ducos, 1995).}

_Thus,

most of the translocations have been identified in animals with a low

prolificacy

(Popescu

and

Boscher,

1986).

The first translocations described involved rather

_large

chromosome

_segments,

and thus could be detected with routine Giemsa stain

_techniques.

The

_peri-

or

paracentric

inversions identified in the

_pig

until now concerned rather small-sized

chromosomal

_segments

and seemed to have no effect on

_reproductive

performance.

For these reasons, the detection of such abnormalities

requires

a

_systematic

_survey

of

_populations

_using

the most elaborate

_cytogenetic

_techniques

_(high

resolution

banding

techniques).

This

_strategy

has been

_developed

in France.

_Today,

all

purebred

boars of the main

_porcine

artificial insemination

centre,

and of one of

the three most

_important

selection groups, are examined

chromosomally

before

they

are

_put

into service. A

_{generalization}

of this

_practice

to all French

_breeding

organizations

is considered essential and should allow us to

complete,

in the near

future,

the current

_(very

_short)

list of identified inversions in the

_{porcine species.}

The

pericentric

inversion of chromosome 4 described in this paper has been

identified

_{independently}

in four

_Large

White

_{purebred boars,}

all

_originating

from different herds. The existence of several ancestors common to these

_animals,

and

the

apparent

absence of zootechnical

effects,

lead us to think that the

_origin

of the

_abnormality

is rather old and restricted to a small number of

_animals,

from which it

_spread

_considerably

_owing

to the more and more intensive use of artificial

insemination. This

_abnormality

has

not,

so

far,

been found in the other breeds

The results shown in table I seem to indicate a

_slight

favourable effect of the

inversion,

especially

for the

_adiposity

trait.

_Quantitative

trait loci for

_growth

and fatness in

_pigs

have been

_recently

identified on chromosome 4

_(Andersson

et

_al,

1994: the

_QTLs

are linked to the markers

S0001,

S0107 and

S0175,

located on the

pericentric

part

of the

_chromosome).

The modification of the

_{neighbourhood}

_(of

the

_regulation)

of these _genes induced

_by

the inversion could

_{perhaps explain}

the

slight superiority

of carrier animals.

However,

since the effect of the inversion is not

statistically significant,

this

_hypothesis

should be considered _very

_carefully.

The inversion has no

_significant

effect on

_reproductive

performance

of sows sired

by heterozygous

boars.

_Owing

to the _very low number of

_homozygous

carriers

_(only

two

_sows),

the effects of the inversion carried in a

_homozygous

state could not be tested

_{statistically.}

_Although

chance cannot be

_totally

excluded in this

_matter,

the results shown in table II lead us to

_contemplate

an unfavourable effect of

the

_abnormality

in the

_homozygous

females. This effect

_might

be the result of

a modification of the function of certain genes

(Villa

et

_al,

₁₉₉₅₎

that is due to a

change

in their

neighbourhood

(recessive

modification: the environment of the

genes of the two

homologous

chromosomes must be modified so that the effect is

visible).

This

_hypothesis

could be tested

experimentally by

creating

and

_mating

new

homozygous

females. The

_{karyotype analysis}

of a

_large

_sample

of females

_presenting

serious

_problems

of

_{reproduction might}

also allow demonstration of the role of this

inversion,

in a

homozygous

_state,

for certain

_{reproductive impairments.}

The fact that individuals

_heterozygous

for the inversion have a normal

fertility

would seem to indicate that no, or a _very small number of unbalanced

_gametes

are

produced by

these animals. The same

hypothesis

was

_put

forward in the case

of the

_pericentric

inversion of chromosome 1

_{reported by Miyake}

et al

₍₁₉₉₄₎

and contradicts the

_suppositions

of

_Eldridge

₍₁₉₈₅₎

_according

to whom half the number of

gametes

produced by

an individual

heterozygous

for the inversion _carry

duplications/deletions.

A

_{synaptonemal complex analysis}

demonstrated the absence of an inversion

loop

in a

heterozygote

for a

_paracentric

inversion of chromosome

8

_{(Switonski, 1991).}

The

_heterologous

_pairing

observed

_prevents

_{crossing-overs}

inside the inverted

_segment

and is followed

_by

the formation of balanced

_gametes

(Switonski, 1991).

The absence of a

loop

can be

explained by

the small size of

the inverted chromosome

_segment

_(Trunca

and

_Opitz,

_1977;

_Daniel,

_1981;

_Kaiser,

1984),

it is

_{physically impossible}

to form a

_loop;

this was the case for the inversion

described

_by

Switonski

_(1991).

It can also be

_{explained by}

the localization of

the

_breakpoints

_{(Ashley, 1988).}

_According

to

_Perdigo

et al

₍₁₉₈₉₎

inversion

_loops

would

_only

form when the

breakpoints

are localized in

G-negative

(pale)

bands. In

the

_present

case, the inversion involves a rather

_large

chromosome

_segment,

with

breakpoints located,

one in a

_G-negative

band

_(4q2.3)

and the other one at the border of a

_G-positive

band

(4p1.4),

which

_{might explain}

the absence of an inversion

loop.

This

_hypothesis

will soon be

experimentally

tested

by

synaptonemal

complex

analyses.

The

_precise

characterization of this

_abnormality

with the

_help

of classical

cytoge-netic

_techniques

_{(non-molecular)}

is

_relatively

difficult. The structural modification of chromosome 4 due to the inversion is a minor one,

making

its detection very dif

ficult with routine Giemsa stain

_techniques,

and also with the

_RBG-banding

chromosome 4 from the normal chromosome 5 with

_GTG-banding

_(the

band

struc-ture of the inverted chromosome 4 is rather similar to the one of chromosome 5

if the latter is turned

_{upside down;}

the inverted chromosome 4 looks like a

5p

+

).

In order to confirm the

_{initially proposed}

_{interpretation}

_{(fig 3),}

the fluorescent in

situ

_{hybridization}

of

_probes

_marking

the terminal extremities of both arms of chro-mosome 4 was

_programmed.

Several

_probes

were

_judged

as

_potentially

_interesting:

hybrids

of the

_{panel developed by}

Yerle et al

₍₁₉₉₆₎

and Robic et al

_(1996),

and

one

_cosmid,

BHT12

(Hoyheim

et

_al,

_1994).

The cosmid

_hybridizes

to the

_extremity

of the normal chromosome 4 short arm

(band

4p1.5).

The

_{hybridization}

of this

cos-mid BHT12

_{provided perfectly}

clear results. The

_photos

in

_figure

4 show without

ambiguity

the transfer from the end of the short arm of the inverted chromosome

cytogenetic

observations.

_However,

additional

_{hybridizations}

will be made

_using

other molecular

_probes

_(somatic

cell

_hybrids)

in order to

_support

this

_hypothesis.

ACKNOWLEDGMENTS

We wish to _express our

_gratitude

to the staff of the insemination _centre, of the selection

organizations

as well as the herd-stock

_breeders,

for the

_blood-taking

and all the

arrange-ments

_concerning

the animals. We also thank Dr

_Hoyheim

for

_{kindly providing}

the cosmid

probe,

and the reviewers for their

_helpful

comments on the

_manuscript.

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_{L, Haley CS, Ellegren H,}

Knott

_SA,

Johansson

M,

Andersson

_K,

Andersson-Eklund

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Fredholm

_M,

Hansson

I,

Hakansson

J,

Lundstr6m K

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T

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G-band

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₍₁₉₈₁₎

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Kozubska-Sobocinska

A,

Slota

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