FOLIA UNIVERSITATIS AGRICULTURAE STETINENSIS

FOLIA UNIVERSITATIS AGRICULTURAE STETINENSIS
Folia Univ. Agric. Stetin. 2007, Agricultura, Alimentaria, Piscaria et Zootechnica 253 (1), 85–94
Katarzyna WOJDAK-MAKSYMIEC, Marek KMIEĆ, Sebastian SAPIKOWSKI
ASSOCIATIONS BETWEEN LACTOFERRIN GENE POLYMORPHISM
AND SOMATIC CELL COUNT IN MILK AND MILK PRODUCTION TRAITS
IN JERSEY COWS*
ZWIĄZKI POMIĘDZY POLIMORFIZMEM W GENIE LAKTOFERYNY
A LICZBĄ KOMÓREK SOMATYCZNYCH W MLEKU I CECHAMI
UŻYTKOWOŚCI MLECZNEJ KRÓW RASY JERSEY
Department of Genetics and Animal Breeding, Agricultural University of Szczecin, Poland
ul. Doktora Judyma 6, 72-466 Szczecin, Poland
e-mail: [email protected]
Abstract. The study included a herd of 184 cows of Jersey breed from Wielkopolska region
in Poland. Two alleles of lactoferrin (LTF), A and B, were found in the population. Their frequencies were 0.6522 and 0.3478, respectively. Those alleles determined three genotypes:
AA, BB and AB of the following frequencies: AA – 33.70%, BB – 3.26% and AB – 63.04%. Statistically significant associations were found between somatic cell count (SCC) in milk and LTF
genotype, parity, season, year of study and cow. The highest SCC (transformed to a logarithmic scale) was found in milk of the cows with BB genotype, whereas the lowest one in the cows
with AA genotype. The aim of the study was to searched for possible associations between lactoferrin genotype and daily milk yield as well as fat and protein content in milk. It was found that statistically significant associations exist between lactoferrin genotype and milk production traits.
Key words: Jersey, lactoferrin, milk, polymorphism, somatic cell count.
Słowa kluczowe: jersey, laktoferyna, mleko, polimorfizm, liczba komórek somatycznych.
INTRODUCTION
Mammary infections are one of the most serious problems in dairy cow farming. Every
year, farmers encounter financial losses due to medical expenses and elimination of ill
animals. Milk from infected cows does not qualify for consumption which leads to decreased profits of dairy cow farms.
One of the factors limiting the development of infections is lactoferrin – a component
of mammalian milk, a member of the transferrin family which includes glycoproteins transferring Fe3+ ions. The antimicrobial properties of lactoferrin are attributed to its iron-binding
capacity; removal of iron from the microbial environment eliminates this important microelement that is ultimately needed for the proliferation of microflora (Arnold et al. 1980).
It was shown that many microorganisms express surface receptors for lactoferrin; the binding of lactoferrin to these receptors is accompanied by cell death, which occurs via one
of several mechanisms (e.g. initiation of lipopolysaccharide release from the cell walls) –
Ellison et al. (1988). The bactericidal effect of lactoferrin was demonstrated with respect to
numerous Gram-negative and Gram-positive bacteria. Lactoferrin can also bind some viral
antigens (Yi et al. 1997).
* The study was supported by the Agricultural University of Szczecin, grant No. BW/HB/09/ 2004.
K. Wojdak-Maksymiec et al.
86
Lactoferrin may play a role in the immune response. This protein is a key factor in the
modulation of anti-inflammatory processes by preventing proliferation and differentiation
of immune system cells (Kijlstra 1990). Lactoferrin activates the nonspecific immune response by stimulating phagocytosis and regulates the activity of complement (Zhang and
Lachmann 1996). Due to its characteristics, lactoferrin is one of the most important factors
inhibiting mastitis development in dairy cows. Studies on lactoferrin lead to a conclusion
that its gene can be used as a marker not only for mastitis resistance / susceptibility, but
also as a marker of milk production traits (Sender et al. 2003).
Bovine lactoferrin gene (LTF) was mapped to chromosome 22q24 (Schwerin et al. 1994;
Martin-Burriel et al. 1997). There exists a mutation in the gene sequence that changes
a recognition site for EcoRI restriction enzyme. Seyfert and Kuhn (1994) found two alleles
in lactoferrin locus: A and B and three possible genotypes: AA, AB, and BB.
Somatic cell count (SCC) is a good early diagnostic indicator of subclinical and acute
forms of mastitis (Harmon 1994; Sender 2002). Genetic correlation between SCC and mastitis was estimated at 0.6–0.97 (Mrode et al. 1998, 1994; Poso and Mantysaari 1996; Van
Dorp 1998). Beside the condition of the mammary gland, SCC also depends on other factors like parity, lactation stage, season and genotype of studied animals (Harmon 1994).
Other authors confirmed significant relation between SCC and milk production (Cameron
and Anderson 1993; Bartlett et al. 1990).
In conclusion, it was reasonable to search for associations between LTF polymorphism
and mastitis resistance / susceptibility and milk production traits.
MATERIAL AND METHODS
The study included a herd of 184 cows of Jersey breed from Wielkopolska region in Poland. All animals were kept in the same environmental conditions. They were fed standard
feed rations and seasonally (in spring and summer) were put out to pasture. The cows
were milked twice a day with the use of a pipeline milking machine. The herd’s milk yield
was evaluated with A4 method in compliance with the recommendations of the International Committee for Animal Recording (ICAR). The data concerning SCC in milk was collected in the years 1998-2002 on the basis of monthly milking tests, representatively sampled from both of the two milkings (2532 samples) performed at the same day time for each
cow. SCC in the samples was determined with an instrumental method in compliance with
the PN-EN ISO/IEC 17025 standard, using Combifoss equipment (Foss, Hillerod, Denmark).
Peripheral blood to be used for DNA isolation was collected from all the cows
and placed in test tubes containing EDTA as anticoagulant. A 301bp fragment was amplified by PCR with the following LTF-specific primers:
F: 5’ – GCC TCA TGA CAA CTC CCA CAC – 3’,
R: 5’ – CAG GTT GAC ACA TCG GTT GAC – 3’.
Primers and PCR conditions were set according to Seyfert and Kühn methodology
(1994). The amplified DNA fragments containing second intron were digested with EcoRI
restrictase and separated on a 2% agarose gel. As a result, different products were obtained: 301bp-long fragment corresponding to allele A (no recognition site for EcoRI)
and a mixture of 201bp and 100bp fragments (allele B).
Associations between lactoferrin gene...
87
The results of LTF locus genotyping were analyzed statistically. Allele and genotype frequencies were calculated and compared to the expected values using χ2 test. Possible associations between LTF polymorphism and SCC were also studied. The following factors
were considered as sources of variability: year of study, season, parity and stage of lactation and cow as nested factor in LTF genotype. The year was divided into four seasons:
winter – from December to February, spring – from March to May, summer – from June to
August and autumn – from September to November. Lactation stages were set as: stage
I – month 1 through 4, stage II – 5 through 8, stage III – month 9 and subsequent months.
Lactation number 5 and subsequent lactations were treated as one category, mainly due
to the decreasing number of available cows of older age and the increasing SCC in milk
in the subsequent lactations. SCC in milk was transformed into a logarithmic scale (natural
logarithm) to equalize the distribution. The following statistic model was applied for calculations:
(ln SCC) yijklm = μ + ai + bj + ck + dl + gm + fn(ai) + eijklmn
where:
yijklm – somatic cell count (ln SCC),
μ – mean somatic cell count for herd (ln SCC),
ai – effect of LTF genotype,
bj – effect of parity,
ck – effect of lactation stage,
dl – effect of season,
gm – effect of study year,
fn(ai) – effect of cow (random, nested factor in LTF genotype),
eijklmn – error.
The results of the analysis were processed statistically according to STATISTICA data
analysis software package, version 6.0 (StatSoft Inc. 2001), with GLM multiple-factor mixed
nested model. Means and standard deviations for different levels of the studied factors
were also calculated.
The influence of LTF genotype on daily milk yield and fat and protein content in milk
in 2002 was also analyzed taking into account season, parity, stage of lactation and cow.
Except for the year of study, the model applied was the same as the one described for
the analysis of associations between LTF genotype and SCC in milk.
RESULTS
Two LTF alleles – A and B were identified in the studied population of cows. The allele
frequencies were found to be 0.6500 and 0.3478, respectively. Three genotypes: AA, AB
and BB were present and their frequencies were as follows: AA – 33.70%, BB – 3.26% and
AB – 63.04% (Table 1). Statistically significant deviations (P ≤ 0.000001) were found between the observed the genotype distribution and the expected one which was estimated
according to the Hardy-Weinberg law. Significantly more AB heterozygotes were present
compared with AA and BB homozygotes. It might have been caused by involuntary selection for the tested trait that could be related to milk production selection.
K. Wojdak-Maksymiec et al.
88
Table 1. Frequencies and distribution of LTF genotypes in the studied population
Tabela 1. Frekwencja i rozkład genotypów LTF w badanej populacji
LTF genotype
Genotyp LTF
Observed frequency
Expected frequency
Frekwencja obserwowana
Frekwencja oczekiwana
N
%
N
%
Chi-square
Chi-kwadrat
AA
62
33.69565
78.2610
42.53308
3.37870
BB
6
3.26086
22.2610
12.09829
11.87818
AB
116
63.04347
83.4780
45.36860
12.67017
Total – Razem
184
100.0000
184.0000
100.00
27.92704
Chi-square – Chi-kwadrat = 27.92704, df = 2, P ≤ 0.000001.
Table 2. Mean values and standard deviations of ln SCC in milk in relation to the level of studied
factors
Tabela 2. Wartości średnie i odchylenia standardowe ln LKS w zależności od poziomu badanych
czynników
Factor
Czynnik
LTF genotype
Gnotyp LTF
Factor level
Poziom czynnika
No. of samples
Liczba prób
Mean ln SCC
Średnia ln SCC
Standard
deviation
Odchylenie standardowe
AA
980
5.124aB
1.132
1471
ac
1.203
Bc
0.966
aB
1.209
aC
1.136
BC
1.133
5.101
A
1.245
5.114
B
1.106
5.360
ABC
1.185
C
1.149
ABd
1.170
Cd
1.180
d
1.094
231
ACd
5.488
1.232
277
5.552BCd
1.077
52
4.325ABCD
1.549
AB
BB
Lactation stage
Stadium laktacji
I
II
III
winter – zima
Season
Sezon
spring – wiosna
summer – lato
autumn – jesień
1.
2.
Parity
Kolejna laktacja
3.
4.
5. and subs.
i kolejne
1998
Year of study
Rok badania
Total – Razem
1999
81
1075
1092
365
391
502
777
862
925
699
400
147
5.246
5.470
5.130
5.203
5.441
5.169
5.070
5.080
5.339
A
1.156
Be
5.383
2000
422
5.404
1.139
2001
537
5.144Ce
1.133
D
2002
1374
5.184
1.162
–
2532
5.206
1.171
The mean marked with the same superscript letter differ significantly – Średnie oznaczone takimi samymi literami różnią się pomiędzy sobą istotnie. Capital letters denote significance of difference at P ≤ 0.01, whereas
small letters denote significance of difference at P ≤ 0.05 – Wielkie litery oznaczają istotność różnic na poziomie
P ≤ 0,01, natomiast małe litery oznaczają istotność na poziomie P ≤ 0,05.
Associations between lactoferrin gene...
89
Statistically significant association was found between SCC and LTF genotype (P ≤ 0.05).
It was also confirmed that statistically significant associations exist between SCC and year
of study (P ≤ 0.001), season (P ≤ 0.01), lactation stage (P ≤ 0.001) and cow (P ≤ 0.001).
The highest SCC (transformed into a logarithmic scale) was recorded in the milk of BB
cows while the lowest one – in AA cows. SCC was generally higher in summer than
in other seasons of the year. Higher SCC was characteristic of the final lactation stage
which includes the drying period when the possibility of developing mastitis increased.
Constant rising tendency in SCC in subsequent lactations was observed – the higher lactation number the higher SCC (Table 2).
Table 3. Mean values of milk production traits in relation to the level of studied factors
Tabela 3. Średnie wartości cech użytkowości mlecznej w zależności od poziomu badanych czynników
Factor
Czynnik
LTF genotype
Gnotyp
LTF
Lactation
stage
Stadium
laktacji
Factor level
Poziom
czynnika
AA
AB
BB
I
Total
Razem
870
46
561
MS
15.359
a
15.118
b
ab
14.248
4.068
0.568
1.058
4.126
0.553
Ac
1.105
4.248
0.596
AB
0.794
3.701
0.411
Bc
5.852
6.055
0.945
4.288
0.414
1.078
4.653
0.526
ABc
1.073
4.298
0.647
B
0.900
3.889
0.550
Ad
0.809
3.928
0.426
cd
0.978
4.323
0.525
Abcd
13.445
AB
16.625
BC
439
0.989
bc
5.755
6.634Ac
BC
461
SD
6.040
10.604
summer – lato
4.763
MS
3.208
13.665
221
252
4.693
SD
Ab
3.251
617
spring – wiosna
4.731
MS
Protein content
Zawartość białka
[%]
18.630
II
247
SD
Fat content
Zawartość tłuszczu
[%]
AB
III
autumn – iesień
Parity
Kolejna
laktacja
483
Daily milk yield
Dobowa wydajność
mleka [kg]
AC
winter – zima
Season
Sezon
No.
of samples
Liczba prób
AD
15.781
14.672
CD
aBCD
4.120
4.743
5.212
4.389
4.338
5.270
6.516
5.671
5.274
6.105
1.
456
13.230
4.049
5.668
1.007
4.028
0.601
2.
404
15.380ae
4.498
5.875b
1.036
4.171
0.548
4.936
c
1.078
4.148
0.551
d
1.012
4.093
0.479
A
3.
4.
5. and subs.
i kolejne
–
240
128
B
16.707
Ce
17.463
171
15.994
1399
15.173
D
4.442
5.894
5.830
4.834
6.028
1.036
4.144
0.526
4.709
5.825
1.038
4.110
0.561
Explanations see Table 2 – Objaśnienia zob. tab. 2.
Associations between milk production traits (daily milk yield and fat and protein content)
and LTF genotype and other factors (lactation stage, parity, season and cow) were also
studied. All the factors were found to be statistically significant for daily milk yield and fat
content, whereas in the case of protein content only cow was found to be a significant factor. Table 3 shows mean values of milk production traits in relation to the studied factors.
The highest daily milk yield was found in cows with AA LTF genotype while the lowest
one was characteristic of animals with BB genotype. Fat and protein content was found
to be related to the lactoferrin genotype the other way round – the highest values were
reached by animals with BB genotype, the lowest – with AA genotype.
K. Wojdak-Maksymiec et al.
90
Daily milk yield was increasing up to the 4th lactation and then started to decrease. Daily
milk yield was higher in summer and the lowest in winter. Lactation stage was also found
to have a significant influence on milk yield which was the highest in first and the lowest
in third lactation stage. In subsequent seasons, lactations and lactation stages, higher milk
yield was accompanied by lower fat and protein content. This fact is well known as a negative correlation exists between milk yield and fat and protein content.
DISCUSSION
The results obtained in this study correspond to those reported by Seyfert and Kühn
(1994), who found two alleles A and B with frequencies of 0.755 and 0.245 (respectively),
which encoded three genotypes. The only difference is that allele A was found to have
a slightly higher frequency in this study.
The results can confirm the hypothesis that LTF gene product is involved in the mechanism of mammary gland immune response during mastitis. The same conclusion was also
drawn by other authors.
Lactoferrin is involved particularly in alimentary immunity (Schutz et al. 1994; Seyfert
et al. 1997; Kanyshkova et al. 2001). This immunity results from the fact that possible infection factors have a limited availability of iron (as well as other growth agents, such as phosphorus and zinc), since its concentration in organism fluids is reduced (Persson
et al. 1992). Another function of lactoferrin is to inhibit enteric absorption of iron in neonates.
Lactoferrin may also take part in intracellular destruction of bacteria by inducing hydroxyl
radical formation, which is catalyzed by iron (Fang and Oliver 1999). Lactoferrin appears in
infected areas also due to its local synthesis (Senft and Neudecker 1991; Persson
et al. 1992). For example, infection of the mammary gland results in a 30-fold increase
in the synthesis of lactoferrin in the secretory cells of the gland (Kawai et al. 1999). In addition, LTF stimulates the immune system and serves as a natural antioxidant (Detilleux 2002).
Lactoferrin may be active in the modulation and regulation of macrophage, lymphocyte and
neutrophil functions (Sordillo et al. 1997). Due to its properties, lactoferrin is one
of the most important factors that prevent and control mastitis in dairy cows and LTF gene
is a candidate marker of SCC in milk (Klussmann and Seyfert 1995; Klussmann et al. 1996;
Seyfert et al. 1996; Hirvonen et al. 1999; Klungland et al. 2001; Teng 2002).
Furthermore, the results of this study prove that SCC is associated with other factors
(year of study, lactation stage, parity, season and cow). Similar associations between SCC
in milk and lactation number (age), herd, breed and lactation stage (days elapsed from
calving) were reported by other authors (Laevens et al. 1997; Busato et al. 2000). Analogous results for lactation number, lactation stage and breed effect on SCC were also reported by Schutz et al. (1994) and Cameron and Anderson (1993). On the other hand,
Nikodémusz et al. (1994) recorded maximum SCC in the milk of HF and Hungarian RedSpotted cows in the first month of lactation. In the second month, SCC remained high,
and afterwards it decreased in the subsequent months to grow again from the 7th month
on. The highest level of SCC in the first month of lactation was not confirmed in this study.
Associations between lactoferrin gene...
91
It was determined in this study that SCC is generally lowest in winter and highest
in summer, which coincides with an increased incidence of clinical mastitis during the
summer months. Smith et al. (1985) also showed that the rate of infection with environmental pathogens was highest during the summer and coincided with the highest number
of coliforms in bedding. The authors suggested that the stress of high temperatures
and humidity could have increased susceptibility to infection as well as increased the number of pathogens to which cows were exposed. These findings support the concept that
temperature stress per se is not the cause of increased SCC, but the increased SCC
is a result of greater exposure of teat ends to pathogens, resulting in more new infections
and clinical cases during the summer months.
CONCLUSIONS
The results obtained in this study confirm the hypothesis that LTF gene can be used
as a marker of somatic cell count in milk and, in consequence, as a marker of susceptibility/resistance to mastitis in dairy cows. Additional studies on this problem, however,
are necessary to confirm associations between lactoferrin genotype and SCC before this
criterion is used in large-scale selection.
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Streszczenie. Badaniami objęto stado 184 krów rasy jersey hodowanych w Wielkopolsce.
W badanej populacji stwierdzono występowanie dwóch alleli laktoferyny – A i B. Ich frekwencja wynosiła odpowiednio 0,6522 i 0,3478. Kontrolowały one obecność trzech genotypów: AA, BB i AB o częstości odpowiednio: 33,70, 3,26 i 63,04%. Stwierdzono istnienie
statystycznie istotnych związków pomiędzy liczbą komórek somatycznych a genotypem
LTF, kolejną laktacją, sezonem, rokiem badania i krową. Największa liczba komórek somatycznych (transformowana na skalę logarytmiczną) została odnotowana w mleku krów
o genotypie BB, zaś najmniejsza – u krów o genotypie AA. W badaniach stwierdzono także statystycznie istotne związki pomiędzy genotypem laktoferyny a dobową wydajnością
mleczną oraz procentową zawartością tłuszczu i białka w mleku.