Chromosome-pairing in trisomic spermatocytes of males with normal or altered karyotypes

HAL Id: hal-00893935

https://hal.archives-ouvertes.fr/hal-00893935

Submitted on 1 Jan 1991

HAL is a multi-disciplinary open access

archive for the deposit and dissemination of

sci-entific research documents, whether they are

pub-lished or not. The documents may come from

teaching and research institutions in France or

abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est

destinée au dépôt et à la diffusion de documents

scientifiques de niveau recherche, publiés ou non,

émanant des établissements d’enseignement et de

recherche français ou étrangers, des laboratoires

publics ou privés.

Chromosome-pairing in trisomic spermatocytes of males

with normal or altered karyotypes

M Świtoński, G Stranzinger, Pk Basrur, Rm Kenney

To cite this version:

Chromosome-pairing

in

trisomic

_{spermatocytes}

of males

with

normal

or

altered

karyotypes

M

&jadnr;wito&jadnr;ski

G

_Stranzinger

₂

PK Basrur

3

RM

_Kenney

1

Academy of Agriculture, Wolyn7iska 3,!,

Pl-60-637

Pozna

?

i,

Poland;

2

Federal Institute

of Technology,

Tannenstr 1, CH-8092

Zurich, Switzerland;

Universit! of Guelph,

Ontario

_Veterinary

College,

Guelph,

Ontario N1G

2W1, Canada;

University of Pennsylvania,

New Bolton

_Center,

PA

_19348,

USA

(Proceedings

of the 9th

European Colloquium

on

_Cytogenetics

of Domestic

Animals;

Toulouse-Auzeville,

10-13

_{July 1990)}

meiosis

_/

synaptonemal complexes

/

aneuploidy

/

trisomy

/

domestic animals

INTRODUCTION

Chromosome studies carried out in domestic mammals show that

_aneuploidy

is rare

compared

to structural chromosomal aberrations.

_Among

the cases of

aneuploidy

reported,

the most

_frequent

is the monosomy XO

syndrome

in mares

(Cribiu,

_1984;

Long,

1988).

There are also identified cases of

_trisomy

X in cows

_(Pinheiro

et

_al,

1987),

the XXY

_syndrome

in bulls

_(Sysa

and

_Slota,

₁₉₈₄₎

and autosomal trisomics

(Herzog

et

_al,

_1977;

Mdkinen et

_{al, 1987;}

Klunder et

_al,

_1989).

The low

_frenquency

of

aneuploidy

in domestic mammals is attributable to

sev-eral factors.

_Aneuploidy

often causes

lethality

or

_major

malformations

_affecting

the

viability

of carriers. Malformed animals are,

therefore,

usually

culled

by

breeders

without recourse to

_{cytogenetic investigation.}

If animals

_{carrying aneuploid}

kary-otypes

are

_{viable, they}

are often sterile. Unlike structural

_{rearrangements}

which are

inherited,

this

_type

of chromosomal aberration cannot be

_spread

in a

population

due to the

_sterility

of the carriers.

_Therefore,

it is safe to assume that all identified cases of

_aneuploidy

were of de novo

_origin.

In the

_present

_study,

we show

that,

_{among germ} cells of the males with normal

and altered

_karyotypes,

trisomic

_{spermatocytes}

can occur

regardless

of the somatic

MATERIALS AND METHODS

The

_samples

of testicular tissue were collected from 3 males with

_recognized

karyotypes:

1)

a normal

bull, 60,XY;

2)

a stallion

_diagnosed

as

_being

_{sterile, 64,XY;}

and

₃₎

a balanced Robertsonian translocation-carrier

_goat

buck, 59,XY

rob

(3/7).

Analyses

of

_synaptonemal

_complexes

were carried out

_by

the

_application

of

the ’whole mount’ surface

_spreading

technique

(Counce

and

_Meyer,

_1973).

The

analytical procedure

described

_by

Switonski

et al

₍₁₉₈₇₎

was followed.

Spermatocytes

were observed with

_Philips

210 and Joel 100S electron

micro-scopes.

RESULTS

Altogether,

79

_primary

_{spermatocytes}

were examined for

synaptonemal

complexes

(table I).

Among

these, 22,

33 and 24 cells were from the

_bull,

the stallion and

the

_{buck, respectively.}

In each of these

_animals,

one

_spermatocyte

was noted to be

trisomic, representing 4.5,

3.0 and

4.2%

of the total number of

_{spermatocytes}

analyzed

from these 3

animals,

respectively.

In the case of the

_bull,

the trivalent detected in the trisomic

_spermatocyte

was medium-sized

(fig 1).

One of these chromosomes was

_{partly aligned}

with the

completely synapsed

bivalent.

However,

the central element between the bivalent

and the third chromosome was not detectable. The third chromosome was thicker

and had a stranded appearance

typical

of the

unpaired

chromosomal

segments.

The trivalent found in the sterile stallion

_represented

a small-sized acrocentric

chromosome

_{(fig 2).}

A combination of

_{pairing possibilities}

was illustrated

by

this

trivalent. The middle

_part

of the trivalent showed

triple pairing

with 2

_parallel

central elements. At both distal

_ends,

2 out of 3 lateral elements were

synapsed,

while the third one remained

unpaired.

Again,

the

unpaired

_segments

were thicker

and

_stranded,

as described above for the bull’s trivalent. In

addition,

in some

_parts

of this

_trivalent,

all 3 lateral elements also remained

_unpaired.

The trivalent found in the buck’s

_spermatocyte

was

_relatively

short

(fig

3),

it had

an even contour and a

_regular

appearance and all lateral elements were

_completely

DISCUSSION

On the basis of the

_present

observations on trisomic

_{spermatocytes,}

it can be

surmised that chromosomal

_{non-disjunction}

occurred in

_{spermatogonia}

of the

animals

_investigated

at a

frequency

of _up to

4.5%.

Spontaneous

occurrence of

trisomic

_{spermatocytes}

has also been described

by

other authors. Dollin and

_Murray

(1984)

reported

one trisomic

_spermatocyte

_among the 16 cells

analyzed

(6.2%)

in a bull.

Analyses

of

synaptonemal

complexes

in Sitka deer mouse

(Hale

and

Greenbaum,

1986)

showed 7 trisomic

_{spermatocytes}

with an XXY set _among

422 cells

_(1.6%)

studied from 3 animals. The above-mentioned studies on the

of such events

_ranging

from 1.6 to

6.2.%

are in

_agreement

with the

_finding

of a

recent

_{investigation}

on the

_frequency

of

aneuploidy

in human _sperm

_(Martin

and

Rademaker,

1990).

These authors found that the overall

frequency

of

aneuploidy

was

3.9%,

however,

cases of

_hypohaploid

_sperm were more

frequent

(3.3%)

than

the

_hyperhaploid

ones

_(0.7%).

Pairing

behavior of trivalents in a trisomic situation can _vary

_{considerably.}

In

our

_study,

we found a

_variety

of

_pairing

behaviors:

1)

an

_alignment

of the third

chromosome

_along

the

_synapsed

bivalent without

_forming

a central

_element,

₂₎

partial pairing

between all 3 partners with formation of central elements between

2 or 3 lateral

elements,

and

₃₎

_{complete triple pairing}

_forming

2

_parallel

central

elements. A varied

_pairing

behavior of trivalents was also observed in studies on

study,

the trivalent _very often

_(in

50%

of observed

_cells)

was associated or

_paired

with the sex bivalent.

Identification of

_{non-disjunction}

events at different levels of

_{gametogenesis}

can

improve

our

_knowledge

on the mechanisms

_responsible

for the occurrence of

chromosomally

unbalanced

_gametes

and

_embryos.

The

_spontaneous

occurrence of

trisomic

primary

spermatocytes

shows in our animals and those discussed above

that chromosomal

_{non-disjunction}

in

_{spermatogonia}

_plays

an

_important

role in

REFERENCES

Counce

_{SJ, Meyer}

GF

₍₁₉₇₃₎

Differentiation of the

_{synaptonemal complex}

and the

kinetochore in Locusta _{spermatocytes} studied

by

whole mount electron

_microscopy.

Chromosoma 44, 231-253

Cribiu EP

₍₁₉₈₄₎

_(auelques

cas de

_dysg6n6sie

_gonadique

chez la

_jument

causes _par

difr6rentes aberrations

_gonosomiques

_(monosomie

_{X, mosaique}

_X/XX

et _caryotype

_XY).

G6n6t S61 Evol _16, 397-404

Dollin

AI;, Murray

JD

_{(1984) Triple}

chromosome

_pairing

in an

aneuploid

bull

spermato-cyte. Can J Genet

_Cytol

26, 782-783

Hate DB-V, Greenbaum IF

₍₁₉₈₆₎

Spontaneous

occurrence ofXXY

primary

spermatocytes in the Silka deer mouse. J Hered 77, 131-132

Herzog A,

Hohn 1-I, Rieck GW

₍₁₉₇₇₎

Survey

of recent situation of chromosome

_pathology

in different breeds of German cattle. Ann G6n6t Sel Anim 9, 471-491

I<lunder LR,

NIcFeely RA,

Beech J, McClune W, Bilinski WF

₍₁₉₈₉₎

Autosomal

trisomy

in a standard bred colt.

_Equine

Vet J 21, 69-79

Long

SE

₍₁₉₈₈₎

Chromosome anomalies and

_infertility

in the mare.

_Equine

Vet

J 20, 89-93

Mlakinen _A, Alitalo I, Alanco M

₍₁₉₈₇₎

Autosomal

_trisomy

in a heifer. Acta Vet

Scand 28,

1-8

Martin

_RI-I,

Rademaker A

₍₁₉₉₀₎

The

_{frequency of aneuploidy}

among individual chromo-somes in 6821 human _sperm chromosome

_{complements. Cytogenet}

Cell Genet

53,

103-107

Pinheiro

_LEL,

Almeida

_IL,

Garcia

_JN,

Basrur PK

_{(1987) Trisomy}

X and

_1/29

translocation

in infertile heifers.

Theriogenetics

28, 891-898

Switonski

M, Gustavsson

_I,

P16en L

₍₁₉₈₇₎

The nature of the _1;29 translocation in cattle as revealed

_{by synaptonemal complex analysis using}

electron

_microscopy.

_Cytogenet

Cell

Genet 44,

103-111

1

Sysa PS,

Slota E

₍₁₉₈₄₎

The XXY

_syndrome

in cattle. 6th

_{European Colloquiurrc}

on

Cylogenetics of Domestic

Animals

_{(Zurich). (Sranzinger}

_G,

_ed)

120-128

Waiiace

_GN4N,

Hulten MA

₍₁₉₈₃₎

_Triple

chromosome

_synapsis

in _oocytes from a human