Alterations of protein glycosylation in embryonic stem cells during adipogenesis

Liu,Wenguang; Yan,Xingrong; Liu,Wei; Wang,Yangyang; Rao,Yang; Yu,Hanjie; Cui,Jihong; Xie,Xin; Sun,Mei; Yin,Lu; Li,Hongmin; Chen,Fulin

doi:10.3892/ijmm.2017.3240

Alterations of protein glycosylation in embryonic stem cells during adipogenesis

Authors:
- Wenguang Liu
- Xingrong Yan
- Wei Liu
- Yangyang Wang
- Yang Rao
- Hanjie Yu
- Jihong Cui
- Xin Xie
- Mei Sun
- Lu Yin
- Hongmin Li
- Fulin Chen
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Affiliations: Faculty of Life Sciences, Northwest University, Xi'an, Shaanxi 710069, P.R. China
Published online on: November 7, 2017 https://doi.org/10.3892/ijmm.2017.3240
Pages: 293-301
Copyright: © Liu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

The understanding of adipose tissue development is crucial for the treatment of obesity-related diseases. Adipogenesis has been extensively investigated at the gene and protein levels in recent years. However, the alterations in protein glycosylation during this process remains unknown, particularly that of parthenogenetic embryonic stem cells (pESCs), a type of ESCs with low immunogenicity and no ethical concerns regarding their use. Protein glycosylation markedly affects cell growth and development, cell-to-cell communication, tumour growth and metastasis. In the present study, the adipogenic potentials of J1 ESCs and pESCs were first compared and the results demonstrated that pESCs had lower adipogenic potential compared with J1 ESCs. Lectin microarray was then used to screen the alteration of protein glycosylation during adipogenesis. The results revealed that protein modification of GlcNAc and α-1-2-fucosylation increased, whereas α-1-6‑fucosylation, α-2-6-sialylation and α-1-6-mannosylation decreased in J1 ESCs and pESCs during this process. In addition, α-1-3-mannosylation decreased only in pESCs. Lectin histochemistry and quantitative polymerase chain reaction of glycosyltransferase confirmed the results obtained by lectin microarray. Therefore, protein glycosylation of ESCs was significantly altered during adipogenesis, indicating that protein glycosylation analysis is not only helpful for studying the mechanism of adipogenesis, but may also be used as a marker to monitor adipogenic development.

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1	Shepherd PR, Gnudi L, Tozzo E, Yang H, Leach F and Kahn BB: Adipose cell hyperplasia and enhanced glucose disposal in transgenic mice overexpressing GLUT4 selectively in adipose tissue. J Biol Chem. 268:22243–22246. 1993.PubMed/NCBI
2	Wolfgang MJ and Lane MD: Control of energy homeostasis: role of enzymes and intermediates of fatty acid metabolism in the central nervous system. Annu Rev Nutr. 26:23–44. 2006. View Article : Google Scholar : PubMed/NCBI
3	Dani C, Smith AG, Dessolin S, Leroy P, Staccini L, Villageois P, Darimont C and Ailhaud G: Differentiation of embryonic stem cells into adipocytes in vitro. J Cell Sci. 110:1279–1285. 1997.PubMed/NCBI
4	Tang QQ, Otto TC and Lane MD: Commitment of C3H10T1/2 pluripotent stem cells to the adipocyte lineage. Proc Natl Acad Sci USA. 101:9607–9611. 2004. View Article : Google Scholar : PubMed/NCBI
5	Serrero G and Lepak NM: Prostaglandin F2alpha receptor (FP receptor) agonists are potent adipose differentiation inhibitors for primary culture of adipocyte precursors in defined medium. Biochem Biophys Res Commun. 233:200–202. 1997. View Article : Google Scholar : PubMed/NCBI
6	Bowers RR, Kim JW, Otto TC and Lane MD: Stable stem cell commitment to the adipocyte lineage by inhibition of DNA methylation: role of the BMP-4 gene. Proc Natl Acad Sci USA. 103:13022–13027. 2006. View Article : Google Scholar : PubMed/NCBI
7	Bowers RR and Lane MD: Wnt signaling and adipocyte lineage commitment. Cell Cycle. 7:1191–1196. 2008. View Article : Google Scholar : PubMed/NCBI
8	Spinella-Jaegle S, Rawadi G, Kawai S, Gallea S, Faucheu C, Mollat P, Courtois B, Bergaud B, Ramez V, Blanchet AM, et al: Sonic hedgehog increases the commitment of pluripotent mesenchymal cells into the osteoblastic lineage and abolishes adipocytic differentiation. J Cell Sci. 114:2085–2094. 2001.PubMed/NCBI
9	van der Horst G, Farih-Sips H, Löwik CW and Karperien M: Hedgehog stimulates only osteoblastic differentiation of undifferentiated KS483 cells. Bone. 33:899–910. 2003. View Article : Google Scholar : PubMed/NCBI
10	MacDougald OA and Lane MD: Transcriptional regulation of gene expression during adipocyte differentiation. Annu Rev Biochem. 64:345–373. 1995. View Article : Google Scholar : PubMed/NCBI
11	Student AK, Hsu RY and Lane MD: Induction of fatty acid synthetase synthesis in differentiating 3T3-L1 preadipocytes. J Biol Chem. 255:4745–4750. 1980.PubMed/NCBI
12	Darlington GJ, Ross SE and MacDougald OA: The role of C/EBP genes in adipocyte differentiation. J Biol Chem. 273:30057–30060. 1998. View Article : Google Scholar : PubMed/NCBI
13	Ailhaud G, Grimaldi P and Négrel R: Cellular and molecular aspects of adipose tissue development. Annu Rev Nutr. 12:207–233. 1992. View Article : Google Scholar : PubMed/NCBI
14	Apweiler R, Hermjakob H and Sharon N: On the frequency of protein glycosylation, as deduced from analysis of the SWISS-PROT database. Biochim Biophys Acta. 1473:4–8. 1999. View Article : Google Scholar : PubMed/NCBI
15	Lowe JB and Marth JD: A genetic approach to mammalian glycan function. Annu Rev Biochem. 72:643–691. 2003. View Article : Google Scholar : PubMed/NCBI
16	Hwang HY, Olson SK, Esko JD and Horvitz HR: Caenorhabditis elegans early embryogenesis and vulval morphogenesis require chondroitin biosynthesis. Nature. 423:439–443. 2003. View Article : Google Scholar : PubMed/NCBI
17	Crocker PR: Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signalling. Curr Opin Struct Biol. 12:609–615. 2002. View Article : Google Scholar : PubMed/NCBI
18	Collins BE and Paulson JC: Cell surface biology mediated by low affinity multivalent protein-glycan interactions. Curr Opin Chem Biol. 8:617–625. 2004. View Article : Google Scholar : PubMed/NCBI
19	Liu D, Shriver Z, Venkataraman G, El Shabrawi Y and Sasisekharan R: Tumor cell surface heparan sulfate as cryptic promoters or inhibitors of tumor growth and metastasis. Proc Natl Acad Sci USA. 99:568–573. 2002. View Article : Google Scholar : PubMed/NCBI
20	Sasisekharan R, Shriver Z, Venkataraman G and Narayanasami U: Roles of heparan-sulphate glycosaminoglycans in cancer. Nat Rev Cancer. 2:521–528. 2002. View Article : Google Scholar : PubMed/NCBI
21	Muramatsu T and Muramatsu H: Carbohydrate antigens expressed on stem cells and early embryonic cells. Glycoconj J. 21:41–45. 2004. View Article : Google Scholar : PubMed/NCBI
22	Qin Y, Zhong Y, Dang L, Zhu M, Yu H, Chen W, Cui J, Bian H and Li Z: Alteration of protein glycosylation in human hepatic stellate cells activated with transforming growth factor-β1. J Proteomics. 75:4114–4123. 2012. View Article : Google Scholar : PubMed/NCBI
23	Ito H, Kuno A, Sawaki H, Sogabe M, Ozaki H, Tanaka Y, Mizokami M, Shoda J, Angata T, Sato T, et al: Strategy for glycoproteomics: identification of glyco-alteration using multiple glycan profiling tools. J Proteome Res. 8:1358–1367. 2009. View Article : Google Scholar : PubMed/NCBI
24	Yu H, Zhu M, Qin Y, Zhong Y, Yan H, Wang Q, Bian H and Li Z: Analysis of glycan-related genes expression and glycan profiles in mice with liver fibrosis. J Proteome Res. 11:5277–5285. 2012. View Article : Google Scholar : PubMed/NCBI
25	Hwang NS, Kim MS, Sampattavanich S, Baek JH, Zhang Z and Elisseeff J: Effects of three-dimensional culture and growth factors on the chondrogenic differentiation of murine embryonic stem cells. Stem Cells. 24:284–291. 2006. View Article : Google Scholar
26	Chen Y, Ai A, Tang ZY, Zhou GD, Liu W, Cao Y and Zhang WJ: Mesenchymal-like stem cells derived from human parthenogenetic embryonic stem cells. Stem Cells Dev. 21:143–151. 2012. View Article : Google Scholar
27	Scillitani G, Zizza S, Liquori GE and Ferri D: Lectin histochemistry of gastrointestinal glycoconjugates in the greater horseshoe bat, Rhinolophus ferrumequinum (Schreber, 1774). Acta Histochem. 109:347–357. 2007. View Article : Google Scholar : PubMed/NCBI
28	Moremen KW, Tiemeyer M and Nairn AV: Vertebrate protein glycosylation: diversity, synthesis and function. Nat Rev Mol Cell Biol. 13:448–462. 2012. View Article : Google Scholar : PubMed/NCBI
29	Sasaki N, Okishio K, Ui-Tei K, Saigo K, Kinoshita-Toyoda A, Toyoda H, Nishimura T, Suda Y, Hayasaka M, Hanaoka K, et al: Heparan sulfate regulates self-renewal and pluripotency of embryonic stem cells. J Biol Chem. 283:3594–3606. 2008. View Article : Google Scholar
30	Satomaa T, Heiskanen A, Mikkola M, Olsson C, Blomqvist M, Tiittanen M, Jaatinen T, Aitio O, Olonen A, Helin J, et al: The N-glycome of human embryonic stem cells. BMC Cell Biol. 10:422009. View Article : Google Scholar : PubMed/NCBI
31	Paffoni A, Brevini TA, Gandolfi F and Ragni G: Parthenogenetic activation: biology and applications in the ART laboratory. Placenta. 29(Suppl B): 121–125. 2008. View Article : Google Scholar : PubMed/NCBI
32	Kim K, Lerou P, Yabuuchi A, Lengerke C, Ng K, West J, Kirby A, Daly MJ and Daley GQ: Histocompatible embryonic stem cells by parthenogenesis. Science. 315:482–486. 2007. View Article : Google Scholar
33	Didié M, Christalla P, Rubart M, Muppala V, Döker S, Unsöld B, El-Armouche A, Rau T, Eschenhagen T, Schwoerer AP, et al: Parthenogenetic stem cells for tissue-engineered heart repair. J Clin Invest. 123:1285–1298. 2013. View Article : Google Scholar : PubMed/NCBI