Proteomic analysis of adipose tissue during the last weeks of gestation in pure and crossbred Large White or Meishan fetuses gestated by sows of either breed
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摘要
Background: The degree of adipose tissue development at birth may influence neonatal survival and subsequent health outcomes. Despite their lower birth weights, piglets from Meishan sows(a fat breed with excellent maternal ability) have a higher survival rate than piglets from Large White sows(a lean breed). To identify the main pathways involved in subcutaneous adipose tissue maturation during the last month of gestation, we compared the proteome and the expression levels of some genes at d 90 and d 110 of gestation in purebred and crossbred Large White or Meishan fetuses gestated by sows of either breed.Results: A total of 52 proteins in fetal subcutaneous adipose tissue were identified as differential y expressed over the course of gestation. Many proteins involved in energy metabolism were more abundant, whereas some proteins participating in cytoskeleton organization were reduced in abundance on d 110 compared with d 90. Irrespective of age,24 proteins differed in abundance between fetal genotypes, and an interaction effect between fetal age and genotype was observed for 13 proteins. The abundance levels of proteins known to be responsive to nutrient levels such as aldolase and fatty acid binding proteins, as wel as the expression levels of FASN, a key lipogenic enzyme, and MLXIPL, a pivotal transcriptional mediator of glucose-related stimulation of lipogenic genes, were elevated in the adipose tissue of pure and crossbred fetuses from Meishan sows. These data suggested that the adipose tissue of these fetuses had superior metabolic functionality, whatever their paternal genes. Conversely, proteins participating in redox homeostasis and apoptotic cel clearance had a lower abundance in Meishan than in Large White fetuses. Time-course differences in adipose tissue protein abundance were revealed between fetal genotypes for a few secreted proteins participating in responses to organic substances, such as alpha-2-HS-glycoprotein, transferrin and albumin.Conclusions: These results underline the importance of not only fetal age but also maternal intrauterine environment in the regulation of several proteins in subcutaneous adipose tissue. These proteins may be used to estimate the maturity grade of piglet neonates.
Background: The degree of adipose tissue development at birth may influence neonatal survival and subsequent health outcomes. Despite their lower birth weights, piglets from Meishan sows(a fat breed with excellent maternal ability) have a higher survival rate than piglets from Large White sows(a lean breed). To identify the main pathways involved in subcutaneous adipose tissue maturation during the last month of gestation, we compared the proteome and the expression levels of some genes at d 90 and d 110 of gestation in purebred and crossbred Large White or Meishan fetuses gestated by sows of either breed.Results: A total of 52 proteins in fetal subcutaneous adipose tissue were identified as differential y expressed over the course of gestation. Many proteins involved in energy metabolism were more abundant, whereas some proteins participating in cytoskeleton organization were reduced in abundance on d 110 compared with d 90. Irrespective of age,24 proteins differed in abundance between fetal genotypes, and an interaction effect between fetal age and genotype was observed for 13 proteins. The abundance levels of proteins known to be responsive to nutrient levels such as aldolase and fatty acid binding proteins, as wel as the expression levels of FASN, a key lipogenic enzyme, and MLXIPL, a pivotal transcriptional mediator of glucose-related stimulation of lipogenic genes, were elevated in the adipose tissue of pure and crossbred fetuses from Meishan sows. These data suggested that the adipose tissue of these fetuses had superior metabolic functionality, whatever their paternal genes. Conversely, proteins participating in redox homeostasis and apoptotic cel clearance had a lower abundance in Meishan than in Large White fetuses. Time-course differences in adipose tissue protein abundance were revealed between fetal genotypes for a few secreted proteins participating in responses to organic substances, such as alpha-2-HS-glycoprotein, transferrin and albumin.Conclusions: These results underline the importance of not only fetal age but also maternal intrauterine environment in the regulation of several proteins in subcutaneous adipose tissue. These proteins may be used to estimate the maturity grade of piglet neonates.
Background: The degree of adipose tissue development at birth may influence neonatal survival and subsequent health outcomes. Despite their lower birth weights, piglets from Meishan sows(a fat breed with excellent maternal ability) have a higher survival rate than piglets from Large White sows(a lean breed). To identify the main pathways involved in subcutaneous adipose tissue maturation during the last month of gestation, we compared the proteome and the expression levels of some genes at d 90 and d 110 of gestation in purebred and crossbred Large White or Meishan fetuses gestated by sows of either breed.Results: A total of 52 proteins in fetal subcutaneous adipose tissue were identified as differential y expressed over the course of gestation. Many proteins involved in energy metabolism were more abundant, whereas some proteins participating in cytoskeleton organization were reduced in abundance on d 110 compared with d 90. Irrespective of age,24 proteins differed in abundance between fetal genotypes, and an interaction effect between fetal age and genotype was observed for 13 proteins. The abundance levels of proteins known to be responsive to nutrient levels such as aldolase and fatty acid binding proteins, as wel as the expression levels of FASN, a key lipogenic enzyme, and MLXIPL, a pivotal transcriptional mediator of glucose-related stimulation of lipogenic genes, were elevated in the adipose tissue of pure and crossbred fetuses from Meishan sows. These data suggested that the adipose tissue of these fetuses had superior metabolic functionality, whatever their paternal genes. Conversely, proteins participating in redox homeostasis and apoptotic cel clearance had a lower abundance in Meishan than in Large White fetuses. Time-course differences in adipose tissue protein abundance were revealed between fetal genotypes for a few secreted proteins participating in responses to organic substances, such as alpha-2-HS-glycoprotein, transferrin and albumin.Conclusions: These results underline the importance of not only fetal age but also maternal intrauterine environment in the regulation of several proteins in subcutaneous adipose tissue. These proteins may be used to estimate the maturity grade of piglet neonates.
引文
1.Gondret F,Lefaucheur L,Juin H,Louveau I,Lebret B.Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs.J Anim Sci.2006;84:93-103.
2.Hales CN,Barker DJ,Clark PM,Cox LJ,Fall C,Osmond C,et al.Fetal and infant growth and impaired glucose tolerance at age 64.BMJ.1991;303:1019-22.
3.Morrison JL,Duffield JA,Muhlhausler BS,Gentili S,Mc Millen IC.Fetal growth restriction,catch-up growth and the early origins of insulin resistance and visceral obesity.Pediatr Nephrol.2010;25:669-77.
4.National Research Council.Preterm Birth:Causes,Consequences,and Prevention.Washington,DC:The National Academies Press;2007.Richard E.Behrman,Adrienne Stith Butler,Editors,Committee on Understanding Premature Birth and Assuring Healthy Outcomes.792 pages.978-0-309-10159-2
5.GTTT.2015.[Résultats Porcs Bretagne].Agricultures&Territoires.Chambres d’Agriculture Bretagne.
6.Leenhouwers JI,Knol EF,de Groot PN,Vos H,van der Lende T.Fetal development in the pig in relation to genetic merit for piglet survival.JAnim Sci.2002;80:1759-70.
7.Canario L,Père MC,Tribout T,Thomas F,David C,GoguéJ,et al.Estimation of genetic trends from 1977 to 1998 of body composition and physiological state of large white pigs at birth.Animal.2007;1:1409-13.
8.Morise A,Sève B,MacéK,Magliola C,Le Hu?rou-luron I,Louveau I.Impact of intrauterine growth retardation and early protein intake on growth,adipose tissue,and the insulin-like growth factor system in piglets.Pediatr Res.2009;65:45-50.
9.Rehfeldt C,Lefaucheur L,Block J,Stabenow B,Pfuhl R,Otten W,et al.Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets.Eur J Nutr.2012;51:151-65.
10.Le Dividich J,Mormède P,Catheline M,Caritez JC.Body composition and cold resistance of the neonatal pig from European(large white)and Chinese(Meishan)breeds.Biol Neonate.1991;59:268-77.
11.Herpin P,Le Dividich J,Amaral N.Effect of selection for lean tissue growth on body composition and physiological state of the pig at birth.J Anim Sci.1993;71:2645-53.
12.Mersmann HJ,Pond WG,Stone RT,Yen JT,Lindvall RN.Factors affecting growth and survival of neonatal genetically obese and lean swine:cross fostering experiments.Growth.1984;48:209-20.
13.Stone RT,Campion DR,Klindt J,Martin RJ.Blood parameters and body composition in fetuses from reciprocal crosses of genetically lean and obese swine.Proc Soc Exp Biol Med.1985;180:191-5.
14.Louveau I,Perruchot MH,Bonnet M,Gondret F.Invited review:Pre-and postnatal adipose tissue development in farm animals:from stem cells to adipocyte physiology.Animal.2016 Nov;10:1839-47.
15.Canario L,Cantoni E,Le Bihan E,Caritez JC,Billon Y,Bidanel JP,et al.Between-breed variability of stillbirth and its relationship with sow and piglet characteristics.J Anim Sci.2006;84:3185-96.
16.Hausman GJ,Poulos SP,Richardson RL,Barb CR,Andacht T,Kirk HC,et al.Secreted proteins and genes in fetal and neonatal pig adipose tissue and stromal-vascular cells.J Anim Sci.2006;84:1666-81.
17.Gondret F,Guitton N,Guillerm-Regost C,Louveau I.Regional differences in porcine adipocytes isolated from skeletal muscle and adipose tissues as identified by a proteomic approach.J Anim Sci.2008;86:2115-25.
18.Gondret F,Guével B,Com E,Vincent A,Lebret B.A comparison of subcutaneous adipose tissue proteomes in juvenile piglets with a contrasted adiposity underscored similarities with human obesity.J Proteome.2012;75:949-61.
19.Guo J,Liu Z,Sun H,Huang Y,Albrecht E,Zhao R,et al.Lipopolysaccharide challenge significantly influences lipid metabolism and proteome of white adipose tissue in growing pigs.Lipids Health Dis.2015;14:68.
20.Voillet V,San Cristobal M,Lippi Y,Martin PG,Iannuccelli N,Lascor C,et al.Muscle transcriptomic investigation of late fetal development identifies candidate genes for piglet maturity.BMC Genomics.2014;15:797.
21.Xu H,Wilcox D,Nguyen P,Voorbach M,Suhar T,Morgan SJ,et al.Hepatic knockdown of mitochondrial GPAT1 in ob/ob mice improves metabolic profile.Biochem Biophys Res Commun.2006;349:439-48.
22.Sarr O,Louveau I,Kalbe C,Metges CC,Rehfeldt C,Gondret F.Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets.J Anim Sci.2010;88:1626-41.
23.Gondret F,Père MC,Tacher S,DaréS,Trefeu C,Le Hu?rou-Luron I,et al.Spontaneous intra-uterine growth restriction modulates the endocrine status and the developmental expression of genes in porcine fetal and neonatal adipose tissue.Gen Comp Endocrinol.2013;194:208-16.
24.Vandesompele J,De Preter K,Pattyn F,Poppe B,Van Roy N,De Paepe A,et al.Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Genome Biol.2002;3:RESEARCH0034.
25.Noblet J,Dourmad JY,Etienne M.Energy utilization in pregnant and lactating sows:modeling of energy requirements.J Anim Sci.1990;68:562-72.
26.Hill GM,Mahan DC.Essential and nonessential amino acid compositions of the total litter and individual fetal pig content and accretion rates during fetal development.J Anim Sci.2016;94:5239-47.
27.Hausman GJ,Hausman DB.Endocrine regulation of porcine adipose tissue development:cellular and metabolic aspects.In:Hollis GR,editor.Growth of the pig.Wallingford,UK:CAB Int;1993.p.49-74.
28.De Lany JP,Floyd ZE,Zvonic S,Smith A,Gravois A,Reiners E,et al.Proteomic analysis of primary cultures of human adipose-derived stem cells:modulation by adipogenesis.Mol Cell Proteomics.2005;4:731-40.
29.Molina H,Yang Y,Ruch T,Kim JW,Mortensen P,Otto T,et al.Temporal profiling of the adipocyte proteome during differentiation using a five-plex SILAC based strategy.J Proteome Res.2009;8:48-58.
30.Welsh GI,Griffiths MR,Webster KJ,Page MJ,TavaréJM.Proteome analysis of adipogenesis.Proteomics.2004;4:1042-51.
31.Hausman GJ.Cellular and enzyme-histochemical aspects of adipose tissue development in obese(Ossabaw)and lean(crossbred)pig fetuses:an ontogeny study.J Anim Sci.1985;60:1539-51.
32.Hausman GJ,Campion DR,Thomas GB.Adipose tissue cellularity and histochemistry in fetal swine as affected by genetic selection for high or low backfat.J Lipid Res.1983;24:223-8.
33.Hausman GJ,Thomas GB.The development of the inner layer of backfat in fetal and young pigs.J Anim Sci.1984;58:1550-60.
34.Samulin J,Berget I,Lien S,Sundvold H.Differential gene expression of fatty acid binding proteins during porcine adipogenesis.Comp Biochem Physiol B Biochem Mol Biol.2008;151:147-52.
35.Kojima K,Yamamoto K,Irimura T,Osawa T,Ogawa H,Matsumoto I.Characterization of carbohydrate-binding protein p33/41:relation with annexin IV,molecular basis of the doublet forms(p33 and p41),and modulation of the carbohydrate binding activity by phospholipids.J Biol Chem.1996;271:7679-85.
36.Mukherjee R,Yun JW.Long chain acyl Co A synthetase 1 and gelsolin are oppositely regulated in adipogenesis and lipogenesis.Biochem Biophys Res Commun.2012;420:588-93.
37.Gaskins HR,Hausman GJ,Martin RJ.Regulation of gene expression during adipocyte differentiation:a review.J Anim Sci.1989;67:2263-72.
38.Spiegelman BM,Farmer SR.Decreases in tubulin and actin gene expression prior to morphological differentiation of 3T3 adipocytes.Cell.1982;29:53-60.
39.Zhang GH,Lu JX,Chen Y,Guo PH,Qiao ZL,Feng RF,et al.Ch REBP and LXRαmediate synergistically lipogenesis induced by glucose in porcine adipocytes.Gene.2015;565:30-8.
40.Gosmain Y,Dif N,Berbe V,Loizon E,Rieusset J,Vidal H,et al.Regulation of SREBP-1 expression and transcriptional action on HKII and FAS genes during fasting and refeeding in rat tissues.J Lipid Res.2005;46:697-705.
41.Urs S,Smith C,Campbell B,Saxton AM,Taylor J,Zhang B,et al.Gene expression profiling in human preadipocytes and adipocytes by microarray analysis.J Nutr.2004;134:762-70.
42.Qu H,Chen Y,Cao G,Liu C,Xu J,Deng H,et al.Identification and validation of differentially expressed proteins in epithelial ovarian cancers using quantitative proteomics.Oncotarget.2016;7:83187-99.
43.Hausman GJ,Martin RJ.Subcutaneous adipose tissue development in Yorkshire(lean)and Ossabaw(obese)pigs.J Anim Sci.1981;52:1442-9.
44.Mc Beath R,Pirone DM,Nelson CM,Bhadriraju K,Chen CS.Cell shape,cytoskeletal tension,and Rho A regulate stem cell lineage commitment.Dev Cell.2004;6:483-95.
45.Nobes CD,Hall A.Rho,rac and cdc42 GTPases:regulators of actin structures,cell adhesion and motility.Biochem Soc Trans.1995;23:456-9.
46.Lu W,Wang X,Liu J,He Y,Liang Z,Xia Z,et al.Downregulation of ARHGDIAcontributes to human glioma progression through activation of Rho GTPase signaling pathway.Tumour Biol.2016:Oct 10;[Epub ahead of print]
47.Amano M,Ito M,Kimura K,Fukata Y,Chihara K,Nakano T,et al.Phosphorylation and activation of myosin by rho-associated kinase(rho-kinase).J Biol Chem.1996;271:20246-9.
48.Zhang J,Shi Z,Huang J,Zou X.CSTB downregulation promotes cell proliferation and migration and suppresses apoptosis in gastric cancer SGC-7901 cell line.Oncol Res.2016;24:487-94.
49.L'Espérance S,Popa I,Bachvarova M,Plante M,Patten N,Wu L,et al.Gene expression profiling of paired ovarian tumors obtained prior to and following adjuvant chemotherapy:molecular signatures of chemoresistant tumors.Int J Oncol.2006;29:5-24.
50.Gerfault V,Louveau I,Mourot J.The effect of GH and IGF-I on preadipocytes from Large White and Meishan pigs in primary culture.Gen Comp Endocrinol.1999;114:396-404.
51.Louveau I,Gondret F.Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system.Domest Anim Endocrinol.2004;27:241-55.
52.Biensen NJ,Wilson ME,Ford SP.The impact of either a Meishan or Yorkshire uterus on Meishan or Yorkshire fetal and placental development to days 70,90,and 110 of gestation.J Anim Sci.1998;76:2169-76.
53.Caperna TJ,Shannon AE,Blomberg LA,Garrett WM,Ramsay TG.Identification of protein carbonyls in serum of the fetal and neonatal pig.Comp Biochem Physiol B Biochem Mol Biol.2010;156:189-96.
54.Jialal I,Devaraj S,Bettaieb A,Haj F,Adams-Huet B.Increased adipose tissue secretion of Fetuin-a,lipopolysaccharide-binding protein and high-mobility group box protein 1 in metabolic syndrome.Atherosclerosis.2015;241:130-7.
55.Karamessinis PM,Malamitsi-Puchner A,Boutsikou T,Makridakis M,Vougas K,Fountoulakis M,et al.Marked defects in the expression and glycosylation of alpha2-HS glycoprotein/fetuin-a in plasma from neonates with intrauterine growth restriction:proteomics screening and potential clinical implications.Mol Cell Proteomics.2008;7:591-9.
56.Laborda J,Naval J,Calvo M,Lampreave F,Uriel J.Alpha-fetoprotein and albumin uptake by mouse tissues during development.Biol Neonate.1989;56:332-41.
57.Stone RT,Leymaster KA.Relationships of birth weight and pre-nursing concentrations of serum albumin to survival and growth rate in swine.Growth.1985;49:263-70.
58.Stremmel W,Pohl L,Ring A,Herrmann T.A new concept of cellular uptake and intracellular trafficking of long-chain fatty acids.Lipids.2001;36(9):981.
59.Campion DR,Hausman GJ,Stone RT,Klindt J.Influence of maternal obesity on fetal development in pigs.J Anim Sci.1988;66:28-33.
2.Hales CN,Barker DJ,Clark PM,Cox LJ,Fall C,Osmond C,et al.Fetal and infant growth and impaired glucose tolerance at age 64.BMJ.1991;303:1019-22.
3.Morrison JL,Duffield JA,Muhlhausler BS,Gentili S,Mc Millen IC.Fetal growth restriction,catch-up growth and the early origins of insulin resistance and visceral obesity.Pediatr Nephrol.2010;25:669-77.
4.National Research Council.Preterm Birth:Causes,Consequences,and Prevention.Washington,DC:The National Academies Press;2007.Richard E.Behrman,Adrienne Stith Butler,Editors,Committee on Understanding Premature Birth and Assuring Healthy Outcomes.792 pages.978-0-309-10159-2
5.GTTT.2015.[Résultats Porcs Bretagne].Agricultures&Territoires.Chambres d’Agriculture Bretagne.
6.Leenhouwers JI,Knol EF,de Groot PN,Vos H,van der Lende T.Fetal development in the pig in relation to genetic merit for piglet survival.JAnim Sci.2002;80:1759-70.
7.Canario L,Père MC,Tribout T,Thomas F,David C,GoguéJ,et al.Estimation of genetic trends from 1977 to 1998 of body composition and physiological state of large white pigs at birth.Animal.2007;1:1409-13.
8.Morise A,Sève B,MacéK,Magliola C,Le Hu?rou-luron I,Louveau I.Impact of intrauterine growth retardation and early protein intake on growth,adipose tissue,and the insulin-like growth factor system in piglets.Pediatr Res.2009;65:45-50.
9.Rehfeldt C,Lefaucheur L,Block J,Stabenow B,Pfuhl R,Otten W,et al.Limited and excess protein intake of pregnant gilts differently affects body composition and cellularity of skeletal muscle and subcutaneous adipose tissue of newborn and weanling piglets.Eur J Nutr.2012;51:151-65.
10.Le Dividich J,Mormède P,Catheline M,Caritez JC.Body composition and cold resistance of the neonatal pig from European(large white)and Chinese(Meishan)breeds.Biol Neonate.1991;59:268-77.
11.Herpin P,Le Dividich J,Amaral N.Effect of selection for lean tissue growth on body composition and physiological state of the pig at birth.J Anim Sci.1993;71:2645-53.
12.Mersmann HJ,Pond WG,Stone RT,Yen JT,Lindvall RN.Factors affecting growth and survival of neonatal genetically obese and lean swine:cross fostering experiments.Growth.1984;48:209-20.
13.Stone RT,Campion DR,Klindt J,Martin RJ.Blood parameters and body composition in fetuses from reciprocal crosses of genetically lean and obese swine.Proc Soc Exp Biol Med.1985;180:191-5.
14.Louveau I,Perruchot MH,Bonnet M,Gondret F.Invited review:Pre-and postnatal adipose tissue development in farm animals:from stem cells to adipocyte physiology.Animal.2016 Nov;10:1839-47.
15.Canario L,Cantoni E,Le Bihan E,Caritez JC,Billon Y,Bidanel JP,et al.Between-breed variability of stillbirth and its relationship with sow and piglet characteristics.J Anim Sci.2006;84:3185-96.
16.Hausman GJ,Poulos SP,Richardson RL,Barb CR,Andacht T,Kirk HC,et al.Secreted proteins and genes in fetal and neonatal pig adipose tissue and stromal-vascular cells.J Anim Sci.2006;84:1666-81.
17.Gondret F,Guitton N,Guillerm-Regost C,Louveau I.Regional differences in porcine adipocytes isolated from skeletal muscle and adipose tissues as identified by a proteomic approach.J Anim Sci.2008;86:2115-25.
18.Gondret F,Guével B,Com E,Vincent A,Lebret B.A comparison of subcutaneous adipose tissue proteomes in juvenile piglets with a contrasted adiposity underscored similarities with human obesity.J Proteome.2012;75:949-61.
19.Guo J,Liu Z,Sun H,Huang Y,Albrecht E,Zhao R,et al.Lipopolysaccharide challenge significantly influences lipid metabolism and proteome of white adipose tissue in growing pigs.Lipids Health Dis.2015;14:68.
20.Voillet V,San Cristobal M,Lippi Y,Martin PG,Iannuccelli N,Lascor C,et al.Muscle transcriptomic investigation of late fetal development identifies candidate genes for piglet maturity.BMC Genomics.2014;15:797.
21.Xu H,Wilcox D,Nguyen P,Voorbach M,Suhar T,Morgan SJ,et al.Hepatic knockdown of mitochondrial GPAT1 in ob/ob mice improves metabolic profile.Biochem Biophys Res Commun.2006;349:439-48.
22.Sarr O,Louveau I,Kalbe C,Metges CC,Rehfeldt C,Gondret F.Prenatal exposure to maternal low or high protein diets induces modest changes in the adipose tissue proteome of newborn piglets.J Anim Sci.2010;88:1626-41.
23.Gondret F,Père MC,Tacher S,DaréS,Trefeu C,Le Hu?rou-Luron I,et al.Spontaneous intra-uterine growth restriction modulates the endocrine status and the developmental expression of genes in porcine fetal and neonatal adipose tissue.Gen Comp Endocrinol.2013;194:208-16.
24.Vandesompele J,De Preter K,Pattyn F,Poppe B,Van Roy N,De Paepe A,et al.Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Genome Biol.2002;3:RESEARCH0034.
25.Noblet J,Dourmad JY,Etienne M.Energy utilization in pregnant and lactating sows:modeling of energy requirements.J Anim Sci.1990;68:562-72.
26.Hill GM,Mahan DC.Essential and nonessential amino acid compositions of the total litter and individual fetal pig content and accretion rates during fetal development.J Anim Sci.2016;94:5239-47.
27.Hausman GJ,Hausman DB.Endocrine regulation of porcine adipose tissue development:cellular and metabolic aspects.In:Hollis GR,editor.Growth of the pig.Wallingford,UK:CAB Int;1993.p.49-74.
28.De Lany JP,Floyd ZE,Zvonic S,Smith A,Gravois A,Reiners E,et al.Proteomic analysis of primary cultures of human adipose-derived stem cells:modulation by adipogenesis.Mol Cell Proteomics.2005;4:731-40.
29.Molina H,Yang Y,Ruch T,Kim JW,Mortensen P,Otto T,et al.Temporal profiling of the adipocyte proteome during differentiation using a five-plex SILAC based strategy.J Proteome Res.2009;8:48-58.
30.Welsh GI,Griffiths MR,Webster KJ,Page MJ,TavaréJM.Proteome analysis of adipogenesis.Proteomics.2004;4:1042-51.
31.Hausman GJ.Cellular and enzyme-histochemical aspects of adipose tissue development in obese(Ossabaw)and lean(crossbred)pig fetuses:an ontogeny study.J Anim Sci.1985;60:1539-51.
32.Hausman GJ,Campion DR,Thomas GB.Adipose tissue cellularity and histochemistry in fetal swine as affected by genetic selection for high or low backfat.J Lipid Res.1983;24:223-8.
33.Hausman GJ,Thomas GB.The development of the inner layer of backfat in fetal and young pigs.J Anim Sci.1984;58:1550-60.
34.Samulin J,Berget I,Lien S,Sundvold H.Differential gene expression of fatty acid binding proteins during porcine adipogenesis.Comp Biochem Physiol B Biochem Mol Biol.2008;151:147-52.
35.Kojima K,Yamamoto K,Irimura T,Osawa T,Ogawa H,Matsumoto I.Characterization of carbohydrate-binding protein p33/41:relation with annexin IV,molecular basis of the doublet forms(p33 and p41),and modulation of the carbohydrate binding activity by phospholipids.J Biol Chem.1996;271:7679-85.
36.Mukherjee R,Yun JW.Long chain acyl Co A synthetase 1 and gelsolin are oppositely regulated in adipogenesis and lipogenesis.Biochem Biophys Res Commun.2012;420:588-93.
37.Gaskins HR,Hausman GJ,Martin RJ.Regulation of gene expression during adipocyte differentiation:a review.J Anim Sci.1989;67:2263-72.
38.Spiegelman BM,Farmer SR.Decreases in tubulin and actin gene expression prior to morphological differentiation of 3T3 adipocytes.Cell.1982;29:53-60.
39.Zhang GH,Lu JX,Chen Y,Guo PH,Qiao ZL,Feng RF,et al.Ch REBP and LXRαmediate synergistically lipogenesis induced by glucose in porcine adipocytes.Gene.2015;565:30-8.
40.Gosmain Y,Dif N,Berbe V,Loizon E,Rieusset J,Vidal H,et al.Regulation of SREBP-1 expression and transcriptional action on HKII and FAS genes during fasting and refeeding in rat tissues.J Lipid Res.2005;46:697-705.
41.Urs S,Smith C,Campbell B,Saxton AM,Taylor J,Zhang B,et al.Gene expression profiling in human preadipocytes and adipocytes by microarray analysis.J Nutr.2004;134:762-70.
42.Qu H,Chen Y,Cao G,Liu C,Xu J,Deng H,et al.Identification and validation of differentially expressed proteins in epithelial ovarian cancers using quantitative proteomics.Oncotarget.2016;7:83187-99.
43.Hausman GJ,Martin RJ.Subcutaneous adipose tissue development in Yorkshire(lean)and Ossabaw(obese)pigs.J Anim Sci.1981;52:1442-9.
44.Mc Beath R,Pirone DM,Nelson CM,Bhadriraju K,Chen CS.Cell shape,cytoskeletal tension,and Rho A regulate stem cell lineage commitment.Dev Cell.2004;6:483-95.
45.Nobes CD,Hall A.Rho,rac and cdc42 GTPases:regulators of actin structures,cell adhesion and motility.Biochem Soc Trans.1995;23:456-9.
46.Lu W,Wang X,Liu J,He Y,Liang Z,Xia Z,et al.Downregulation of ARHGDIAcontributes to human glioma progression through activation of Rho GTPase signaling pathway.Tumour Biol.2016:Oct 10;[Epub ahead of print]
47.Amano M,Ito M,Kimura K,Fukata Y,Chihara K,Nakano T,et al.Phosphorylation and activation of myosin by rho-associated kinase(rho-kinase).J Biol Chem.1996;271:20246-9.
48.Zhang J,Shi Z,Huang J,Zou X.CSTB downregulation promotes cell proliferation and migration and suppresses apoptosis in gastric cancer SGC-7901 cell line.Oncol Res.2016;24:487-94.
49.L'Espérance S,Popa I,Bachvarova M,Plante M,Patten N,Wu L,et al.Gene expression profiling of paired ovarian tumors obtained prior to and following adjuvant chemotherapy:molecular signatures of chemoresistant tumors.Int J Oncol.2006;29:5-24.
50.Gerfault V,Louveau I,Mourot J.The effect of GH and IGF-I on preadipocytes from Large White and Meishan pigs in primary culture.Gen Comp Endocrinol.1999;114:396-404.
51.Louveau I,Gondret F.Regulation of development and metabolism of adipose tissue by growth hormone and the insulin-like growth factor system.Domest Anim Endocrinol.2004;27:241-55.
52.Biensen NJ,Wilson ME,Ford SP.The impact of either a Meishan or Yorkshire uterus on Meishan or Yorkshire fetal and placental development to days 70,90,and 110 of gestation.J Anim Sci.1998;76:2169-76.
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