Growth and Blood Constituents of Immature New Hampshire Fowl Exposed to a Constant Temperature of 99°F. for 7 Days
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Institute of Nutrition of Central America and Panama (JNCAP), Guatemala, C. A
Received September 3, 1958.
The effect of high environmental temperatures on mortality, growth, feed consumption and thyroid weights of immature fowl
fed ad libitum has been reported by Wilson and Plaister (1951) and Joiner and Huston (1957). In the studies presented here the effect on
growth and blood serum sconstituents of 5-week old New Hampshire chicks maintained at a constant temperature of 99°F. for
a 7-day period has been determined for both ad libitum and paired feeding regimens.
The equipment used for these high temperature studies has been previously described (Squibb et al., 1954). The New Hampshire chicks used in these experiments were F1 female progeny from imported stock. The control birds were housed in all-wire cages in a room having a temperature of 70°F.
The effects of an environmental temperature of 99°F. was studied under two feeding regimens: (1) ad libitum, and (2) paired. All birds were fed an imported mash containing . . .
Poultry Science
10.3382/ps.0380220
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Very Short Introductions
World's ClassicsPMCID: PMC4143640Genetic Diversity in the Prion Protein Gene (PRNP) of
Domestic Cattle and Water Buffaloes in Vietnam, Indonesia and Thailand,1 ,5 ,6 ,7 ,3 ,4 ,2 and
1,*2)Laboratory of Food Microbiology and Food Safety, School of Veterinary Medicine, Rakuno Gakuen University, Ebetsu, Hokkaido 069&#x, Japan3)Laboratory of Veterinary Hygiene, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Hokkaido 060&#x, Japan4)Department of Veterinary Medicine, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183&#x, Japan5)National Veterinary Drug Assay Laboratory, Indonesia6)Department of Veterinary Microbiology, Faculty of Veterinary Science, Chulalongkorn University, Thailand7)Department of Veterinary Hygiene, National Institute of Veterinary Research, Hanoi, Vietnam*Correspondence to: Muramatsu, Y., Laboratory of Zoonotic Diseases, School of Veterinary Medicine, Rakuno Gakuen University, 582 Bunkyodai-Midorimachi, Ebetsu, Hokkaido 069-8501, Japan. e-mail:
This article has been
other articles in PMC.There has been an accumulation of information on frequencies of insertion/deletion
(indel) polymorphisms within the bovine prion protein gene (PRNP) and on
the number of octapeptide repeats and single nucleotide polymorphisms (SNPs) in the coding
region of bovine PRNP related to bovine spongiform encephalopathy (BSE)
susceptibility. We investigated the frequencies of 23-bp indel polymorphism in the
promoter region (23indel) and 12-bp indel polymorphism in intron 1 region (12indel),
octapeptide repeat polymorphisms and SNPs in the bovine PRNP of cattle
and water buffaloes in Vietnam, Indonesia and Thailand. The frequency of the deletion
allele in the 23indel site was significantly low in cattle of Indonesia and Thailand and
water buffaloes. The deletion allele frequency in the 12indel site was significantly low
in all of the cattle and buffaloes categorized in each subgroup. In both indel sites, the
deletion allele has been reported to be associated with susceptibility to classical BSE.
In some Indonesian local cattle breeds, the frequency of the allele with 5 octapeptide
repeats was significantly high despite the fact that the allele with 6 octapeptide repeats
has been reported to be most frequent in many breeds of cattle. Four SNPs observed in
Indonesian local cattle have not been reported for domestic cattle. This study provided
information on PRNP of livestock in these Southeast Asian countries.Keywords: BSE, indel polymorphisms, local cattle, PRNP, SNPs, Southeast AsiaGenomic DNA samples from cattle and water buffalo in Vietnam, Thailand and
Indonesia: We collected liver or spleen samples from 288 cattle (Bos
taurus and B. indicus) and 60 water buffalo (Swamp buffalo,
Bubalus bubalis) in Vietnam, Indonesia and Thailand ( and ). Vietnamese samples were collected from nine provinces in the northern part of
Vietnam at the period from July to August in 2007. Indonesian samples were collected from
seven provinces in March 2007. For the Thai samples, we bought spleens of cattle and water
buffalo at several grocery stores belonging to three different logistic groups in Bangkok in
December 2005. All of the bovine liver and spleen samples were subjected to extraction of
genomic DNA as described elsewhere []. The
extracted DNA solutions were stored at −30°C until use.Bovinae animals used for this studySampling areas in Vietnam and Thailand (Panel A) and in Indonesia (Panel B). A:
Vietnamese samples (99 cattle and 1 water buffalo) were collected from nine provinces
in the northern part of Vietnam (nos. 1 to 7, Hà Nội and Ninh Binh). ...PCR and sequencing analyses: The extracted DNA solutions were used for PCR
assays to determine the frequencies of polymorphisms within the 23indel, 12indel and
octapeptide repeat regions of bovine PRNP. The primers pair 23F-23R was
used for genotyping 23indel, and the primers pair 12F-12R was used for genotyping 12indel in
each PCR assay []. We designed the primer pair OctF
(5′-GCAACCGTTATCCACCTCAG-3′) and OctR 5′-TGGCTTACTGGGTTTGTTCC-3′) for PCR to amplify the octapeptide repeat region
on the basis of the sequence data obtained from GenBank (Acc. No. AJ298878). The entire
coding region of PRNP was amplified as two fragments by PCR using the
primer pairs F1-R2 and F2-R1 []. PCRs for the above
four regions were performed with the following conditions of amplification: 2 min at 94°C
followed by 13 cycles of 30 sec each at 94°C, 65°C and 72°C with stepwise lowering of the
annealing temperature from 65°C to 55.4°C by the 13 and 23 cycles of 30 sec each at
94°C, 52°C and 72°C, followed by incubation at 72°C for 5 min as a final extension step. DNA
sequencing was carried out for the PCR products of the entire coding region of
PRNP. Purification of the PCR products for sequencing was done using a
SUPRECTM- PCR (Takara Bio Inc., Otsu, Japan). When the PCR products were
heterozygous for octapeptide repeats in the coding region, the 5-repeat and the 6-repeat
fragments were individually recovered by using a QIAquick Gel Extraction Kit (Qiagen, Tokyo,
Japan). DNA sequencing was carried out in both directions on an ABI PRISMTM 310
Genetic Analyzer using a BigDye&#x000 Terminator v1.1 Cycle Sequencing Kit (Life
Technologies Japan, Tokyo, Japan). Nucleic acid sequences were assembled and edited by using
sequence alignment editing software (BioEdit version 7.0.5,
http://www.mbio.ncsu.edu/bioedit/bioedit.html).Statistical analyses: We categorized all Bovinae animals into 5 groups,
Vietnamese cattle, Indonesian cattle, Thai cattle, Indonesian water buffaloes and Thai water
buffaloes, to determine whether the Hardy-Weinberg equilibrium (HWE) was applicable to the
population in each group. Then, in the 23indel and 12indel polymorphisms, haplotype
frequencies were derived from the genotypic data. The test of HWE and the haplotype
estimation were performed by using gene analysis software, Haploview 4.2
(http://www.broadinstitute.org/scientific-community/science/programs/medical-and-population-genetics/haploview/haploview).
Differences in frequency distributions of allele, genotype and haplotype were calculated
with Fisher’s exact test by using the freely available statistical software ‘EZR’ (version
1.00; Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a
graphical user interface for the free statistical software ‘R’ (version 2.13.0; The R
Foundation for Statistical Computing) []. For
comparison of allelic and genotypic polymorphism frequencies in the 2 indel sites and
haplotype frequency, the following three cattle groups and one water buffalo group were used
as reference groups: UK healthy and BSE-affected Holstein Friesian cattle [], B. indicus of five breeds [] and Anatolian water buffalo (B.
bubalis) []. German healthy and
BSE-affected cattle [] were used as reference
groups for comparison of allelic and genotypic polymorphism frequencies among octapeptide
repeat polymorphisms. Because of the variety of cattle breeds and species, we compared the
frequencies of 23indel, 12indel, haplotype and octapeptide repeat polymorphisms in subgroups
of Indonesian local cattle with those of the reference groups. For comparison among the
subgroups of Indonesian local cattle, information for subgroups with less than 10 head of
cattle was excluded, because the numbers of cattle in these subgroups were too small for
statistical analyses.23indel, 12indel, haplotype and octapeptide repeat polymorphisms (
): The frequency distributions of alleles and genotypes in the
23indel site of Indonesian cattle and Thai cattle were significantly lower than those of all
of the reference cattle groups. However, a significant difference in the frequency
distribution of alleles or genotypes in the 23indel site was not found between Vietnamese
cattle and the UK reference cattle groups. In the 12indel site of cattle, the frequency
distributions were clustered on the ins allele and the ins/ins genotype. The frequencies of
the 12del allele and del/del genotype of the cattle of all three countries were
significantly lower than those of the UK reference cattle groups.Distributions of allele and genotype frequencies for 23-bp indel, 12-bp indel and
octapeptide repeat polymorphisms in PRNP of the bovidae animals
examined in this studyAll of the cattle groups of the three countries showed significant differences in the
frequency distributions of haplotype polymorphisms against all of the reference groups, but
the major haplotype of Vietnamese cattle was different from those of the other 2 countries.
The frequencies of 23del-12del in cattle of all 3 countries were significantly lower than
those in the UK reference cattle groups. The HWE was applicable to all populations for both
indel polymorphisms.In the Indonesian water buffaloes, the frequency distributions of polymorphisms in all
items (indel sites, haplotype and octapeptide repeats) were similar to those of Anatolian
water buffaloes. On the other hand, Thai water buffaloes showed polymorphic patterns of
frequency distributions similar to those of the frequency distributions in Thai cattle for
all items. We excluded information for the Vietnamese water buffalo from , because we tested only one water buffalo in Vietnam in
this study. The genotype and octapeptide repeat polymorphisms of the Vietnamese water
buffalo tested were ins/ins in both indel sites and 6/6. A significant difference between
observed bovine data and reference data was not detected in octapeptide repeat polymorphism.
Seven or more repeats were not detected in our study.Frequencies of 23indel, 12indel, haplotype and octapeptide repeat polymorphisms in
subgroups of Indonesian local cattle (
): In the Kalimantan Selatan local cattle and Bali cattle,
frequencies of the del allele and del/del genotype in both indel sites were significantly
lower than those in all of the reference cattle groups. Significant differences in
frequencies of the 12indel site were found between Peranakan Ongole breed cattle and the UK
reference groups and between Sumatra Utara breed cattle and B. indicus,
respectively. The major haplotypes were 23ins-12ins in Kalimantan Selatan local cattle and
Bali cattle, 23del-12ins in Peranakan Ongole breed and 23del-12del in Sumatra Utara local
cattle. Haplotype 23ins-12del was minor or was not detected. The frequencies of 23del-12del
were significantly lower in all cattle subgroups except Sumatra Utara local cattle than in
the reference groups. The frequencies of 23ins-12ins were significantly higher in Kalimantan
Selatan local cattle and Bali cattle than in the reference groups. For all of the tested
subgroups, the HWE was applicable for the 12indel polymorphism, but was not applicable for
the 23indel polymorphism. As for the frequency of octapeptide repeat polymorphism, only two
subgroups (Kalimantan Selatan local cattle and Bali cattle) showed a significant difference
from the reference groups.Distributions of allele and genotype frequencies for 23-bp indel, 12-bp indel and
octapeptide repeat polymorphisms in PRNP among subgroups of
Indonesian local cattleSingle nucleotide polymorphisms in the coding region of PRNP (): A total of 15 SNPs were detected in the coding region of
PRNP in 85 cattle DNA samples selected from the three countries. All of
the genotypes for octapeptide repeat polymorphism (6/6, 6/5 and 5/5) were included in the
selected samples. Numbering of each nucleotide and amino acid position refers to the
sequence of Bali cattle obtained in this study (GenBank accession no. AB761619). Three sites
at nucleotide positions 8 (A to C), 461 (G to A) and 554 (A to G) were non-silent mutations.
These SNPs corresponded to the following amino acid substitutions: lysine to threonine
(K3T), serine to asparagine (S154N) and asparagine to serine (N185S). Of the remaining 12
SNPs that showed silent mutations, four sites at positions 108 (T to G), 267 (T to A), 554
(A to G) and 783 (C to T) were unique to Indonesian cattle, particularly Kalimantan Selatan
local cattle and Bali cattle. These 4 SNPs have not yet been reported for domestic cattle,
and nucleotide mutation at position 783 (C to T) is known only for Banteng (B.
javanicus) []. There was no
PRNP allele in our samples that exhibited E211K amino acid replacement,
which is considered to be a possible cause of H-type atypical BSE.SNPs in the coding region of bovine PRNP detected in this
studyOur results provide information on PRNP of livestock in these Southeast
Asian countries. Significantly lower frequencies of the del polymorphism in the 23indel site
were found in cattle in Indonesia and Thailand, and significantly lower frequencies of the
del polymorphism in the 12indel site were found in cattle in all three countries. In
contrast, the distributions of 23del polymorphisms in Vietnamese cattle showed a tendency to
be similar to those in the UK reference cattle groups. The breeding history of Vietnamese
cattle may have contributed to the distributional similarity. In Vietnam, more than 80% of
dairy cattle are cross-bred between Holstein Friesian cattle and local Yellow cattle and Red
Sindhi, a B. indicus breed introduced to Vietnam at the beginning of the
20th Century [, ].The frequency patterns of 2 indel polymorphisms in Indonesian cattle and Thai cattle,
especially Bali cattle and Kalimantan Selatan local cattle in Indonesia, do not conform to
any of those previously reported for domestic cattle. These unique genetic backgrounds of
PRNP probably originated from their ancestral animals. Bali cattle are
generally recognized as domesticated cattle from wild Banteng. Bali cattle are different
from all other species of cattle as a result of difference in their origin and evolution.
B. taurus (European breed) and B. indicus (Zebu breed)
are known to have been divided from a common ancestor, Aurochs (Bos
primigenius), more than 3 million years ago. In contrast, restriction fragment
length polymorphisms of mitochondrial DNA and the sequences of mitochondrial genes for
cytochrome b confirmed that B. javanicus had a different ancestor from that
of both B. taurus and B. indicus []. Moreover, a wide gene flow from B. javanicus
extends to Southeast Asian local cattle to varying degrees []. It is notable that the del allele frequencies of two indel polymorphisms were
low in Bali cattle, and our results suggested that both 23del and 12del polymorphisms are
nonexistent or very few in B. javanicus and the ancestral animal of
Southeast Asian local cattle.An association between haplotype frequency for indel polymorphisms and BSE susceptibility
has been reported in some domestic cattle breeds of B. taurus [, ]. The
haplotype 23del-12del, which is associated with BSE incidence, is common in B.
taurus, while the haplotype 23ins-12ins is the major haplotype in Indonesian and
Thai cattle and in water buffalo. Functional studies of the promoter region of bovine
PRNP indicated that 12del results in a significantly low level of
PRNP expression compared with that in the case of 12ins []. However, the frequency of 12del allele is higher in
the population of BSE-affected cattle, because the 12indel site is in strong linkage
disequilibrium with the polymorphism in the 23indel site of PRNP [, , , ]. The
12indel polymorphism of bovine PRNP contains a putative binding region of
SP1, which activates a wide range of viral and cellular genes. The 23-bp insertion leads to
strong and specific binding with RP58, which represses transcription by interfering with the
DNA-binding activity of SP1 []. Therefore,
PRNP expression level is lower in the haplotype 23ins-12ins than in the
haplotype 23del-12del owing to the repressive effect of the haplotype 23ins-12ins [].Although an association between octapeptide repeat polymorphism of bovine
PRNP and typical BSE incidence has not been reported in cattle,
transgenic mice expressing bovine PrPC of which the coding region contains 7 or
10 repeats have been reported to be more susceptible to BSE inoculums [, ]. While most domestic cattle
have 5 or 6 octapeptide repeats [, , , ], seven repeats were reported in at least 5% of Brown
Swiss breed [] and 4 repeats were identified in an
animal of B. indicus × B. taurus composite cattle and 2
domesticated cattle from wild Gaur (Bos gaurus) in Asia, named Mythun
this study, an abnormal number of octapeptide repeats was not detected, but frequencies of
the octapeptide repeat in Bali cattle and Kalimantan Selatan local cattle showed genetic
differences from those of B. taurus and B. indicus.In this study, we detected three non-silent mutations: lysine to threonine (K3T), serine to
asparagine (S154N) and asparagine to serine (N185S). The mutation of K3T, which is located
in a signal sequence of PrP, has been reported to be present in at least 6% of native
Chinese cattle []. Our results suggested the
probability of genetic interchange among Vietnamese local cattle, Kalimantan Selatan local
cattle and native Chinese cattle. On the other hand, the mutation of S154N, which is located
close to the first α-helix [], is a very minor
amino acid replacement in domestic cattle. The replacement has been observed in all alleles
for a wide variety of Bovinae animals (Lesser kudu, Nilgai, Asian water buffalo, Lowland
anoa, African buffalo and Forest buffalo) []. The
mutation of N185S, which is located within the second α-helix [], has not been reported in domestic cattle, but has been confirmed in
B. javanicus and African buffalo []. There has been no report showing an association between the 3 non-silent
mutations and BSE susceptibility. We detected several mutations that were reported in
B. javanicus. The similarity between Bali cattle and B.
javanicus in PRNP polymorphisms supports the hypothesis that
Bali cattle are domesticated from B. javanicus, and our results suggest
that the genetic diversity of PRNP in Indonesian local cattle is a result
of gene flow from B. javanicus.Our results suggest that Southeast Asian cattle and water buffaloes have low susceptibility
to BSE, particularly to classical BSE. In Southeast Asian countries where crossbreeding with
B. taurus and B. indicus has been increasing, selective
improvement in local cattle is important as an approach to provide additional protection
against BSE infection.This work was supported in part by a Grant-in-Aid to Cooperative Research (Rakuno Gakuen
University Dairy Science Institute, 2009-6), a Support Project to Assist Private
Universities in Developing Bases for Research, a Grant-in-Aid for Scientific Research (B)
(grant no. ) and the Program of Founding Research Centers for Emerging and
Reemerging Infectious Diseases, from the MEXT, Japan. This work was also supported by a
grant from the MHLW, Japan (grant no. ).1. Ashbaugh H. R. 2010.
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