|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online January 17, 2007
Journal of Experimental Biology 210, 477-483 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02665
Effect of maternal myostatin antibody on offspring growth performance and body composition in mice
1 Department of Animal Science and Biotechnology, Tunghai University,
Taichung 407, Taiwan, Republic of China,
2 Department of Biotechnology and Bioinformatics, Asia University, Wufeng
Shiang, Taichung 413, Taiwan, Republic of China
3 Life Science Research Center, Tunghai University, Taichung 407, Taiwan,
Republic of China
* Author for correspondence (e-mail: brou{at}thu.edu.tw)
Accepted 22 November 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: myostatin, maternal antibody, growth performance, body composition
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Husmann et al., 1996;
Molkentin and Olson, 1996).
Growth factors such as fibroblast growth factors (FGFs), insulin-like growth
factors (IGFs) and transforming growth factors (TGF-ßs) play important
roles in promoting myogenesis (Musaro et
al., 1999; Semsarian et al.,
1999; Lowe and Always,
1999). The TGF-ß superfamily contains a large group of
secreted growth and differentiation factors that play important roles in
regulation of development and tissue homeostasis
(McPherron and Lee, 1996).
Myostatin, a member of the TGF-ß superfamily, also known as growth
differentiation factor 8 (GDF8), was first identified in mice by McPherron et
al. (McPherron et al., 1997).
Myostatin is the genetic factor for determination of skeletal muscle mass and
weight in the mouse (McPherron et al.,
1997). Furthermore, natural mutations of myostatin caused three
breeds of cattle, Belgium Blue, Piedmontese and Asturiana de los Valles, to
show a double-muscled phenotype (Dunner et
al., 1997; Grobet et al.,
1997; Kambadur et al.,
1997; McPherron and Lee,
1997). It is concluded that myostatin is a negative regulator of
muscle growth. To improve growth performance of animal or livestock, several
molecular strategies and traditional breeding techniques were developed to
manipulate myostatin expression. Myostatin knockout mice and dominant-negative
myostatin mice were reported to enhance growth performance
(McPherron et al., 1997;
Zhu et al., 2000).
Overexpression of myostatin binding protein, follistatin, in transgenic mice
exhibited a more dramatic increase in skeletal muscle mass compared with that
seen in myostatin-knockout mice (Lee and
McPherron, 2001). Injection of anti-myostatin monoclonal blocking
antibody increased skeletal muscle mass in mice
(Bogdanovich et al., 2002).
However, the methods used in all above studies are too complicated,
inefficient and impractical for livestock breeding and production. Thus,
finding a convenient way to improve livestock growth performance by regulating
myostatin expression becomes an important issue.
Immunological memory from the mother plays an important role in regulation
of prenatal and postnatal health. During fetal development, the immune system
is relatively incompetent. Therefore, transferable maternal immunological
memory is essential for the survival of the fetus, newborn and infant.
Maternal adaptive immunity has a strong influence on immune responses in the
fetus and offspring. These antibodies provide passive protection against
infection but also actively shape childhood immunity and tolerance induction
by providing the fetus and infant with maternal immunological experience
(Zinkernagel, 2001;
Uthoff et al., 2003).
Ventura and coworkers demonstrated that anti-Dengue virus Ab existed both
in Dengue virus infected pregnant women and their infants
(Ventura et al., 1975). The
active transplacental transfer of immunoglobulin G (IgG) begins at 6 months of
gestation and increases sharply thereafter. At the end of gestation, IgG
concentrations in fetal serum exceed maternal levels by a ratio of 1.2:1 to
1.8:1 (Sato et al., 1979).
Baker et al. immunized pregnant women with the polysaccharide vaccine of group
B Streptococcus (Baker et al.,
1988). The vaccine-induced IgG was presented in the mother and the
IgG readily crossed the placenta. This evidence indicates that the maternal
antibodies pass freely across the placenta to offspring. Female mice were
immunized with Dermatophagoides pteronyssinus prior to mating with
male mice, and the anti-D. pteronyssinus antibody was found in both
mother and offspring (Victor et al.,
2003).
To improve the growth performance of animals or livestock, maternal adaptive immunity may be a potential alternative protocol to inhibit myostatin activity in fetus and offspring. The objective of this study was to investigate the influence of maternal myostatin antibody on the growth performance and body composition of offspring in mice.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Animals
Specific pathogen-free, 4–5-week-old C57BL/6J mice were used in this
study. Mice were maintained under 23±1°C and 60±5% humidity
with a 12 h:12 h light:dark cycle. Mice were allowed to feed on commercial
mouse chow from a local supplier and to drink ad libitum.
Immunization of mice
The mouse myostatin amino acid sequence was from GenBank (Access No.
NP_034964), and the myostatin antigen peptide was designed by PC Gene
(Barioch, 1995). The peptide
sequence (N'-ECEFVFLQKYP-C') was based upon the hydrophilic region
between 313 and 323 residues near the active site of the myostatin sequence.
Female mice were subcutaneously immunized twice, with a 1-week interval
between immunizations, with 50 µl of an emulsion containing 10 µg of
keyhole limpet hemocyanin (KLH)-conjugated myostatin peptide as antigen in
complete Freund's adjuvant. After 7 days, the mice were immunized twice, with
a 1-week interval between immunizations, with 50 µl of an emulsion
containing 10 µg of KLH-conjugated myostatin peptide in incomplete Freund's
adjuvant. Seven days after the final immunization, dot blotting assay and
ELISA were used to determine the titer of myostatin Ab. The F1 mice were
sacrificed at eight weeks old by cervical dislocation. The flushed body was
weighed and stored at –20°C for body composition analysis.
Determination of antibody titer by ELISA and dot blotting analysis
Purified recombinant myostatin (Liang
et al., 2002) was diluted in 0.05 mol l–1 sodium
carbonate buffer (pH 9.6) containing 100 µg ml–1
recombinant myostatin and coated on a 96-well microtiter plate at 4°C
overnight. The plates were blocked with 200 µl of phosphate-buffered saline
(PBS) containing 2% BSA for 1 h at room temperature and then washed three
times with PBS containing 0.05% Tween 20 (PBS-T). Diluted mouse sera were
added and the plates were incubated for 2 h at room temperature. The
horseradish peroxidase (HRP)-conjugated goat anti-mouse IgG (dilution 1:2000)
was added and then the plates were incubated for 1 h at room temperature.
Following three washes with PBS-T, the ABTS substrate solution was added into
each well. The color changes were monitored using a microplate reader (Bio-Rad
Model 680, Richmond, CA, USA) at a wavelength of 415 nm.
For dot blotting analysis, purified recombinant myostatin was spotted onto nitrocellulose membrane. The blot was incubated for 1 h in 5% skimmed milk in PBS-T at room temperature. Various dilutions of mouse sera were applied to the nitrocellulose membrane followed by 1 h incubation with HRP-conjugated goat anti-mouse IgG. The blot was then washed three times in PBS-T. Specific antibody binding was detected by an ECL detection system.
Analysis of body composition
The carcasses of F1 mice were lyophilized for 48 h. The dried body mass
(Mb,dry) of each mouse was recorded and body water content
was determined by subtracting Mb,dry from flushed body
mass. The carcasses were ground using a Sorvall Omni-Mixer (Sorvall, Newtown,
CT, USA) (Eisen and Leatherwood,
1976). Fat content was determined using the ether extraction
method, and protein content was measured using a Kjeltec Auto Analyzer (FOSS,
Laurel, MD, USA) (Jones,
1984). The water, fat and protein contents were expressed as a
percentage of flushed body mass.
Embryo collection and culture
For embryo collection, the female mice were caged individually with males
and checked for copulation plugs the next morning. Mice were sacrificed by
cervical dislocation and the embryos were flushed from the oviduct. Embryos
were collected and cultured in M199 supplemented with 10% FBS. After culturing
overnight, the development of the embryo was observed by microscopic
examination.
Histological analysis and follicle counting of ovary
The follicle numbers from mouse ovary were determined by histological
analysis according to the method of Lee et al.
(Lee et al., 2004). Ovaries
were fixed in 10% neutral-buffered formalin solution for 24 h at 4°C,
dehydrated, paraffin-embedded and serially sectioned at 5 µm thickness. The
sections were mounted on glass slides and stained with Mayer's hematoxylin
(Sigma Chemical Co.) and eosin. The fifth section of each ovary was used for
follicle counting. Only follicles with a visible nucleus in the oocyte were
counted to avoid duplicate counting of a follicle.
Statistical analysis
Values are presented as means ± standard deviation (s.d.). A
Student's t-test was used to evaluate the differences between the
groups. A significance level of 5% was adopted for the analysis.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
|
To investigate the effect of maternal myostatin Ab on embryo development, the embryos were collected after mating from females in the mstn Ab-induced and control groups. The results showed that the mstn Ab-induced group had significantly fewer embryos than did the control group (P<0.05) (Fig. 2A). After culturing overnight, all embryos from both groups developed normally from the one-cell stage to the two-cell stage (Fig. 2A–E).
|
The effect of myostatin Ab on the development of the follicle in the ovary
was determined by Mayer's hematoxylin and eosin histological staining.
Primordial follicles were defined as those containing flat pregranulosa cells.
Developing follicles including primary and secondary follicles were the
follicles beyond the primordial stage. Primary follicles were those with one
layer of cuboidal follicle cells and secondary follicles were those with two
or more layers of cuboidal cells (Lee et
al., 2004). The results showed that induction of myostatin Ab
increased primordial follicle number and decreased developing follicle number
in ovary (P<0.05) (Fig.
3).
|
|
|
To investigate the effect of maternal myostatin Ab on body composition of offspring, crude protein, crude fat and water content were determined. The results showed that both male and female offspring from the mstn Ab-induced group contained higher crude protein and lower crude fat (P<0.05) (Fig. 6A,B). There was no significant difference in water content of offspring between the mstn Ab-induced and control groups (Fig. 6C).
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Lynch et al., 2001) but also
by negative growth factors such as myostatin
(Bogdanovich et al., 2002;
Wagner et al., 2002).
Myostatin is a member of the TGF-ß superfamily. Animals with myostatin
gene mutation or knockout showed an increase in skeletal muscle mass
(Dunner et al., 1997;
Grobet et al., 1997;
Kambadur et al., 1997;
McPherron and Lee, 1997). The
increase in muscle mass was contributed by the hyperplasia and hypertrophy of
skeletal muscle cells. To improve the growth performance of animals, several
molecular strategies have been developed to manipulate myostatin gene
expression. Mice with a myostatin gene knockout or expression of a
dominant-negative myostatin gene were reported to have enhanced growth
performance (McPherron et al.,
1997; Zhu et al.,
2000). Overexpression of myostatin binding protein, follistatin,
in transgenic mice exhibited a more dramatic increase in skeletal muscle mass
(Lee and McPherron, 2001).
However, these strategies are involved in the alternation of animal genome and
are not practical for livestock breeding and production. Bogdanovich et al.
reported that the blockage of endogenous myostatin by peritoneal injection of
monoclonal antibody for three months resulted in an increase in mice body mass
and that the increased growth performance in animals is due to the hyperplasia
and hypertrophy in skeletal muscle
(Bogdanovich et al., 2002). It
was also reported that recombinant myostatin inhibited the proliferation of
C2C12 mouse myoblasts (Thomas et al.,
2000; Joulia et al.,
2003). During the development of the embryo, expression of
myostatin was detected in day 9.5 post-coitus
(McPherron et al., 1997).
Expression of myostatin in the embryo plays an important role in the
proliferation of muscle cells (Deveaux et
al., 2001). Therefore, repression of myostatin activity in the
embryo is crucial to eliminate the negative effects on animal growth.
Maternal adaptive immunity has a strong influence on the immune responses
of the fetus and offspring. Transplacental antibody transport is a selective
and active process mediated by the Fc receptor. The diaplacental transfer of
IgG might play an important role in offspring immunity
(Uthoff et al., 2003). Kaden
and Lange reported that maternal antibodies produced after oral vaccination of
young female wild boars have a protective effect against classical swine fever
for approximately two months following vaccination
(Kaden and Lange, 2004). In
the current study, the effect of maternal myostatin antibodies on the
offspring growth performance was investigated by active immunization of
myostatin synthetic peptides in female mice before mating.
Female mice immunized with synthetic myostatin peptides produced a high
titer of myostatin Ab (Fig. 1).
The body mass of female mice was not different between the mstn Ab-induced and
control groups (data not shown). These results imply that neutralization of
myostatin by myostatin Ab in mature animals did not affect the further growth
of animals. The litter size and the number of embryos collected from mstn
Ab-induced mice were less than that from the control group
(Fig. 2A). However, the embryos
collected from both groups divided normally into the two-cell stage after
overnight culture (Fig.
2A,D,E). These results indicate that induction of myostatin Ab
reduced the amount of oocytes released from ovary but did not affect the
development of the embryo. Ovary histochemical stain showed that the amount of
developing follicle was reduced in the mstn Ab-induced group
(Fig. 3). These data implied
that myostatin may be involved in the development of follicles in ovary. In
addition, cytokines of the TGF-ß superfamily sharing similar active
sites, such as inhibin and GDF-9 (Pangas
and Matuzk, 2004; Juengel and
McNatty, 2005), are involved in follicle development
(Stock et al., 1997;
Carabatsos et al., 1998;
Elvin et al., 1999). It is
possible that the induction of myostatin Ab may block the action of other
members of the TGF-ß superfamily. Furthermore, in the current study,
synthetic myostatin peptides were conjugated with KLH for amplification of
immune response. To rule out the possible influence of KLH Ab on litter size,
immunization of mice with KLH alone was conducted. The result indicated that
the litter size was similar between KLH immunized and control groups (data not
shown).
The growth performances of both male and female offspring from the mstn
Ab-induced group were higher than those from the control group during the
8-week period (Fig. 5). Owing
to the long half-life of IgG, the 2-month-old offspring of the maternal mstn
Ab-induced group maintained higher myostatin Ab titer than did the control
group based on the ELISA assay (Fig.
4). Due to the negative effect of myostatin on skeletal muscle
growth, reduction of myostatin activity during embryo development and the
newborn stage will cause hyperplasia and hypertrophy of skeletal muscle cells.
This result implies that neutralization of myostatin by maternal Ab affected
the growth performance of offspring. In this study, one week after birth, the
body mass of male offspring in the maternal mstn Ab-induced group was higher
than that in the control group (Fig.
5A). This result may be attributed to the neutralization of
myostatin by maternal myostatin Ab or nutrient limitation of newborn mice in
the control group during the first week after birth. In myostatin-null mice or
negative-dominant myostatin mice, the body mass was higher than in the wild
type (McPherron et al., 1997).
Since myostatin is the negative regulator of muscle growth, inhibition of
myostatin will enhance muscle mass. The increase of muscle mass was
contributed by the increase of crude protein. Offspring from mstn Ab-induced
mice have a lower fat content than those in the control group
(Fig. 6B). It is reported that
myostatin stimulated the adipogenesis of C3H 10T(1/2) mescenchymal multipotent
cells (Artaza et al., 2005).
Increased fat mass in male mice was also observed by overexpression of
myostatin in skeletal muscle
(Reisz-Porszasz et al., 2003).
In conclusion, induction of maternal myostatin Ab resulted in increased crude
protein and decreased fat content in the body composition of offspring. This
provides an animal model to improve livestock production without altering the
genome of the animal. However, owing to the larger animal size, as well as
longer growth and gestation periods, the application of a maternal mstn Ab
strategy in farm animals still needs further investigation.
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Arnold, H. H. and Winter, B. (1998). Muscle differentiation: more complexity to the network of myogenic regulators. Curr. Opin. Genet. Dev. 8, 539-544[CrossRef][Medline]
Artaza, J. N., Bhasin, S., Magee, T. R., Reisz-Porszasz, S.,
Shen, R., Groome, N. P., Fareez, M. M. and Gonzalez-Cadavid, N. F.
(2005). Myostatin inhibits myogenesis and promotes adipogenesis
in C3H 10T(1/2) mesenchymal multipotent cells.
Endocrinology 146,3547
-3557
Baker, C. J., Rench, M. A., Edwards, M. S., Carpenter, R. J., Hays, B. M. and Kasper, D. L. (1988). Immunization of pregnant women with a polysaccharide vaccine of group B streptococcus. N. Engl. J. Med. 319,1180 -1185[Abstract]
Barioch, A. (1995). The Nucleic Acid and Protein Sequence Analysis Software System (PC/GENE). Campbell, CA: IntelliGenetics
Barton, E. R., Morris, L., Musaro, A., Rosenthal, N. and
Sweeney, H. L. (2002). Muscle-specific expression of
insulin-like growth factor I counters muscle decline in mdx mice.
J. Cell Biol. 157,137
-148
Bogdanovich, S., Krag, T. O., Barton, E. R., Morris, L. D., Whittemore, L. A., Ahima, R. S. and Khurana, T. S. (2002). Functional improvement of dystrophic muscle by myostatin blockade. Nature 420,418 -421[CrossRef][Medline]
Carabatsos, M. J., Elvin, J., Matuzk, M. M. and Albertini, D. F. (1998). Characterization of oocyte and follicle development in growth differentiation factor 9 deficient mice. Dev. Biol. 204,373 -384[CrossRef][Medline]
Deveaux, V., Cassar-Malek, I. and Picard, B. (2001). Comparison of contractile characteristics of muscle from Holstein and double-muscled Belgian Blue fetuses. Comp. Biochem. Physiol. 131A,21 -29[CrossRef]
Dunner, S., Chariler, C., Farnir, F., Brouwers, B., Canon, J. and Georges, M. (1997). Towards interbreed IBD fine mapping of the mh locus: double-muscling in Australia de los Valles breed involves the same locus as in Belgian Blue cattle breed. Mamm. Genome 8,430 -435[CrossRef][Medline]
Eisen, E. J. and Leatherwood, J. M. (1976).
Effect of early pregnancy in growth, body composition and efficiency in mice.
J. Anim. Sci. 42,52
-62
Elvin, J. A., Yan, C., Wang, P., Nishimori, K. and Matuzk, M.
M. (1999). Molecular characterization of follicle defects in
growth differentiation factor 9 deficient ovary. Mol.
Endocrinol. 13,1018
-1034
Grobet, L., Martin, L. J., Poncelet, D., Pirottin, D., Brouwers, B., Riquet, J., Schoeberlein, A., Dunner, S., Menissier, F., Massabanda, J. et al. (1997). A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat. Genet. 17, 71-74[CrossRef][Medline]
Husmann, I., Soulet, L., Gautron, J., Martelly, I. and Barritault, D. (1996). Growth factors in skeletal muscle regeneration. Cytokine Growth Factor Rev. 7, 249-258[CrossRef][Medline]
Jones, C. E. (1984). Protein (crude) in animal feed Kjeldahl method. In Official Methods of Analysis of the Association of Official Analytical Chemists (ed. S. Williams), pp. 152-169. Washington, DC: Association of Official Analytical Chemists
Joulia, D., Bernardi, D., Garandel, V., Rabenoelina, F., Vernus, B. and Cabello, G. (2003). Mechanisms involved in the inhibition of myoblast proliferation and differentiation by myostatin. Exp. Cell Res. 286,263 -275[CrossRef][Medline]
Juengel, J. J. and McNatty, K. P. (2005). The role of proteins of transforming growth factor-ß superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 11,143 -160
Kaden, V. and Lange, E. (2004). Development of maternal antibodies after oral vaccination of young female wild boar against classical swine fever. Vet. Microbiol. 103,115 -119[CrossRef][Medline]
Kambadur, R., Sharma, M., Smith, T. P. and Bass, J. J.
(1997). Mutations in myostatin (GDF8) in double-muscled Belgian
Blue and Piedmontese cattle. Genome Res.
7, 910-916
Lee, S. J. and McPherron, A. C. (2001).
Regulation of myostatin activity and muscle growth. Proc. Natl.
Acad. Sci. USA 98,9306
-9311
Lee, W. S., Yoon, S. J., Yoon, T. K., Cha, K. Y., Lee, S. H., Shimaskai, S., Lee, S. and Lee, K. A. (2004). Effect of bone morphogenetic protein-7 (BMP-7) on primordial follicular growth in the mouse ovary. Mol. Reprod. Dev. 69, 159-163[CrossRef][Medline]
Liang, Y. C., Yeh, J. Y. and Ou, B. R. (2002). Overexpression of porcine growth differentiation factor 8 recombinant protein in baculovirus expression system. J. Chin. Soc. Anim. Sci. 31,23 -32
Lowe, D. A. and Always, S. E. (1999). Stretch-induced myogenin, MyoD, and MRF4 expression and acute hypertrophy in quail slow-tonic muscle are not dependent upon satellite cell proliferation. Cell Tissue Res. 296,531 -539[CrossRef][Medline]
Lynch, G. S., Cuffe, S. A., Plant, D. R. and Gregorevic, P. (2001). IGF-1 treatment improves the functional properties of fast- and slow-twitch skeletal muscles from dystrophic mice. Neuromuscul. Disord. 11,260 -268[CrossRef][Medline]
McPherron, A. C. and Lee, S. J. (1996). The transforming growth factor-beta superfamily. In Growth Factors and Cytokines in Health and Disease, vol. 1B (ed. D. LeRoith and C. Bondy), pp. 357-393. Greenwich, CT: JAI Press
McPherron, A. C. and Lee, S. J. (1997). Double
muscling in cattle due to mutations in the myostatin gene. Proc.
Natl. Acad. Sci. USA 94,12457
-12462
McPherron, A. C., Lawler, A. M. and Lee, S. J. (1997). Regulation of skeletal muscle mass in mice by new TGF-beta superfamily member. Nature 387, 83-90[CrossRef][Medline]
Molkentin, J. D. and Olson, E. N. (1996). Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev. 34,169 -206
Musaro, A., McCullagh, K. J., Naya, F. J., Olson, E. N. and Rosenthal, N. (1999). IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400,581 -585[CrossRef][Medline]
Pangas, S. A. and Matuzk, M. M. (2004). Genetic models for transforming growth factor ß superfamily signaling in ovarian follicle development. Mol. Cell. Endocrinol. 255, 83-91
Reisz-Porszasz, S., Bhasin, S., Artaza, J. N., Shen, R.,
Sinha-Hikim, I., Hogue, A., Fielder, J. T. and Gonzalez-Cadavid, N. F.
(2003). Lower skeletal muscle mass in male transgenic mice with
muscle-specific overexpression of myostatin. Am. J. Physiol.
Endocrinol. Metab. 285,E876
-E888
Sato, H., Albrecht, P., Reynolds, D. W., Stagno, S. and Ennis, F. A. (1979). Transfer of measles, mumps, and rubella antibodies from mother to infant. Its effect on measles, mumps, and rubella immunization. Am. J. Dis. Child. 133,1240 -1243[Abstract]
Semsarian, C., Wu, M. J., Ju, U. K., Marciniec, T., Yeoh, T., Allen, D. G., Harvry, R. P. and Graham, R. M. (1999). Skeletal muscle hypertrophy is mediated by a Ca2+-dependent calcineurin signalling pathway. Nature 400,576 -581[CrossRef][Medline]
Stock, A. E., Woodruff, T. K. and Smith, L. C. (1997). Effects of inhibin A and activin A during in vitro maturation of bovine oocytes in hormone- and serum-free medium. Biol. Reprod. 56,1559 -1564[Abstract]
Thomas, M., Langley, B., Berry, C., Sharma, M., Kirk, S., Bass,
J. and Kambadur, R. (2000). Myostatin, a negative regulator
of muscle growth, function by inhibiting myoblast proliferation. J.
Biol. Chem. 275,40235
-40243
Uthoff, H., Spenner, A., Peckelkamm, W., Ahrens, B., Wolk, G.,
Hackler, R., Hardung, F., Schaefer, J., Scheffold, A., Renz, H. et al.
(2003). Critical role of preconceptional immunization for
protective and nonpathological specific immunity in murine neonates.
J. Immunol. 171,3485
-3492
Ventura, A. K., Ehrenkranz, N. J. and Rosenthal, D. (1975). Placental passage of antibody to Dengue virus on person living in a region of hyperendemic Dengue virus infection. J. Infect. Dis. 131,S62 -S68
Victor, J. R., Fusaro, A. E., Duarte, A. J. and Sato, M. N. (2003). Preconception maternal immunization to dust mite inhibits the type I hypersensitivity response of offspring. J. Allergy Clin. Immunol. 111,269 -277[CrossRef][Medline]
Wagner, K. R., McPherron, A. C., Winik, N. and Lee, S. J. (2002). Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann. Neurol. 52, 832-836[CrossRef][Medline]
Zhu, X., Hadhazy, M., Wehling, M., Tidball, J. G. and McNally, E. M. (2000). Dominant negative myostatin produces hypertrophy without hyperplasia in muscle. FEBS Lett. 474, 71-75[CrossRef][Medline]
Zinkernagel, R. M. (2001). Maternal antibodies,
childhood infections, and autoimmune diseases. N. Engl. J.
Med. 345,1331
-1335
This article has been cited by other articles:
|
|
 |
|
  W. Guo, J. Flanagan, R. Jasuja, J. Kirkland, L. Jiang, and S. Bhasin The Effects of Myostatin on Adipogenic Differentiation of Human Bone Marrow-derived Mesenchymal Stem Cells Are Mediated through Cross-communication between Smad3 and Wnt/{beta}-Catenin Signaling Pathways J. Biol. Chem., April 4, 2008; 283(14): 9136 - 9145. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
