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PLOS ONE  2014 

Biphasic Role of Chondroitin Sulfate in Cardiac Differentiation of Embryonic Stem Cells through Inhibition of Wnt/β-Catenin Signaling

DOI: 10.1371/journal.pone.0092381

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Abstract:

The glycosaminoglycan chondroitin sulfate is a critical component of proteoglycans on the cell surface and in the extracellular matrix. As such, chondroitin sulfate side chains and the sulfation balance of chondroitin play important roles in the control of signaling pathways, and have a functional importance in human disease. In contrast, very little is known about the roles of chondroitin sulfate molecules and sulfation patterns during mammalian development and cell lineage specification. Here, we report a novel biphasic role of chondroitin sulfate in the specification of the cardiac cell lineage during embryonic stem cell differentiation through modulation of Wnt/beta-catenin signaling. Lineage marker analysis demonstrates that enzymatic elimination of endogenous chondroitin sulfates leads to defects specifically in cardiac differentiation. This is accompanied by a reduction in the number of beating cardiac foci. Mechanistically, we show that endogenous chondroitin sulfate controls cardiac differentiation in a temporal biphasic manner through inhibition of the Wnt/beta-catenin pathway, a known regulatory pathway for the cardiac lineage. Treatment with a specific exogenous chondroitin sulfate, CS-E, could mimic these biphasic effects on cardiac differentiation and Wnt/beta-catenin signaling. These results establish chondroitin sulfate and its sulfation balance as important regulators of cardiac cell lineage decisions through control of the Wnt/beta-catenin pathway. Our work suggests that targeting the chondroitin biosynthesis and sulfation machinery is a novel promising avenue in regenerative strategies after heart injury.

References

[1]  Habuchi O (2000) Diversity and functions of glycosaminoglycan sulfotransferases. Biochim Biophys Acta 1474: 115–127. doi: 10.1016/s0304-4165(00)00016-7
[2]  Klüppel M (2010) The roles of chondroitin-4-sulfotransferase-1 in development and disease. Prog Mol Biol Transl Sci 93: 113–132. doi: 10.1016/s1877-1173(10)93006-8
[3]  Kusche-Gullberg M, Kjellen L (2003) Sulfotransferases in glycosaminoglycan biosynthesis. Curr Opin Struct Biol 13: 605–611. doi: 10.1016/j.sbi.2003.08.002
[4]  Klüppel M, Vallis KA, Wrana JL (2002) A high-throughput induction gene trap approach defines C4ST as a target of BMP signaling. Mech Dev 118: 77–89. doi: 10.1016/s0925-4773(02)00198-3
[5]  Willis CM, Wrana JL, Klüppel M (2009) Identification and characterization of TGFbeta-dependent and -independent cis-regulatory modules in the C4ST-1/CHST11 locus. Genet Mol Res 8: 1331–1343. doi: 10.4238/vol8-4gmr673
[6]  Klüppel M, Samavarchi-Tehrani P, Liu K, Wrana JL, Hinek A (2012) C4ST-1/CHST11-controlled chondroitin sulfation interferes with oncogenic HRAS signaling in Costello syndrome. European Journal of Human Genetics : EJHG 20: 870–877. doi: 10.1038/ejhg.2012.12
[7]  Klüppel M, Wight TN, Chan C, Hinek A, Wrana JL (2005) Maintenance of chondroitin sulfation balance by chondroitin-4-sulfotransferase 1 is required for chondrocyte development and growth factor signaling during cartilage morphogenesis. Development 132: 3989–4003. doi: 10.1242/dev.01948
[8]  Willis CM, Klüppel M (2012) Inhibition by chondroitin sulfate E can specify functional Wnt/beta-catenin signaling thresholds in NIH3T3 fibroblasts. The Journal of Biological Chemistry 287: 37042–37056. doi: 10.1074/jbc.m112.391490
[9]  Yu P, Pisitkun T, Wang G, Wang R, Katagiri Y, et al. (2013) Global analysis of neuronal phosphoproteome regulation by chondroitin sulfate proteoglycans. PloS one 8: e59285. doi: 10.1371/journal.pone.0059285
[10]  Mizumoto S, Fongmoon D, Sugahara K (2012) Interaction of chondroitin sulfate and dermatan sulfate from various biological sources with heparin-binding growth factors and cytokines. Glycoconjugate Journal. Aug 30(6): 619–32. doi: 10.1007/s10719-012-9463-5
[11]  Asimakopoulou AP, Theocharis AD, Tzanakakis GN, Karamanos NK (2008) The biological role of chondroitin sulfate in cancer and chondroitin-based anticancer agents. In Vivo 22: 385–389.
[12]  Prinz RD, Willis CM, Viloria-Petit A, Klüppel M (2011) Elimination of breast tumor-associated chondroitin sulfate promotes metastasis. Genetics and molecular research : Genet Mol Res 10: 3901–3913. doi: 10.4238/2011.december.8.9
[13]  Theocharis AD, Theocharis DA, De Luca G, Hjerpe A, Karamanos NK (2002) Compositional and structural alterations of chondroitin and dermatan sulfates during the progression of atherosclerosis and aneurysmal dilatation of the human abdominal aorta. Biochimie 84: 667–674. doi: 10.1016/s0300-9084(02)01428-1
[14]  Theocharis AD, Tsara ME, Papageorgacopoulou N, Karavias DD, Theocharis DA (2000) Pancreatic carcinoma is characterized by elevated content of hyaluronan and chondroitin sulfate with altered disaccharide composition. Biochimica et Biophysica Acta 1502: 201–206. doi: 10.1016/s0925-4439(00)00051-x
[15]  Theocharis AD, Tsolakis I, Tzanakakis GN, Karamanos NK (2006) Chondroitin sulfate as a key molecule in the development of atherosclerosis and cancer progression. Advances in pharmacology 53: 281–295. doi: 10.1016/s1054-3589(05)53013-8
[16]  Uebelhart D (2008) Clinical review of chondroitin sulfate in osteoarthritis. Osteoarthritis Cartilage 16 Suppl 3S19–21. doi: 10.1016/j.joca.2008.06.006
[17]  Carulli D, Laabs T, Geller HM, Fawcett JW (2005) Chondroitin sulfate proteoglycans in neural development and regeneration. Current Opinion in Neurobiology 15: 116–120. doi: 10.1016/j.conb.2005.01.014
[18]  Bartus K, James ND, Bosch KD, Bradbury EJ (2012) Chondroitin sulphate proteoglycans: key modulators of spinal cord and brain plasticity. Experimental Neurology 235: 5–17. doi: 10.1016/j.expneurol.2011.08.008
[19]  Bradbury EJ, Carter LM (2011) Manipulating the glial scar: chondroitinase ABC as a therapy for spinal cord injury. Brain Research Bulletin 84: 306–316. doi: 10.1016/j.brainresbull.2010.06.015
[20]  Wang H, Katagiri Y, McCann TE, Unsworth E, Goldsmith P, et al. (2008) Chondroitin-4-sulfation negatively regulates axonal guidance and growth. Journal of Cell Science 121: 3083–3091. doi: 10.1242/jcs.032649
[21]  Purushothaman A, Sugahara K, Faissner A (2012) Chondroitin sulfate “wobble motifs” modulate maintenance and differentiation of neural stem cells and their progeny. The Journal of Biological Chemistry 287: 2935–2942. doi: 10.1074/jbc.r111.298430
[22]  Wilson DG, Phamluong K, Lin WY, Barck K, Carano RA, et al. (2012) Chondroitin sulfate synthase 1 (Chsy1) is required for bone development and digit patterning. Developmental Biology 363: 413–425. doi: 10.1016/j.ydbio.2012.01.005
[23]  Sato T, Kudo T, Ikehara Y, Ogawa H, Hirano T, et al. (2011) Chondroitin sulfate N-acetylgalactosaminyltransferase 1 is necessary for normal endochondral ossification and aggrecan metabolism. The Journal of Biological Chemistry 286: 5803–5812. doi: 10.1074/jbc.m110.159244
[24]  Hermanns P, Unger S, Rossi A, Perez-Aytes A, Cortina H, et al. (2008) Congenital joint dislocations caused by carbohydrate sulfotransferase 3 deficiency in recessive Larsen syndrome and humero-spinal dysostosis. American Journal of Human Genetics 82: 1368–1374. doi: 10.1016/j.ajhg.2008.05.006
[25]  Thiele H, Sakano M, Kitagawa H, Sugahara K, Rajab A, et al. (2004) Loss of chondroitin 6-O-sulfotransferase-1 function results in severe human chondrodysplasia with progressive spinal involvement. Proceedings of the National Academy of Sciences of the United States of America 101: 10155–10160. doi: 10.1073/pnas.0400334101
[26]  Tuysuz B, Mizumoto S, Sugahara K, Celebi A, Mundlos S, et al. (2009) Omani-type spondyloepiphyseal dysplasia with cardiac involvement caused by a missense mutation in CHST3. Clinical Genetics 75: 375–383. doi: 10.1111/j.1399-0004.2009.01167.x
[27]  Uchimura K, Kadomatsu K, Nishimura H, Muramatsu H, Nakamura E, et al. (2002) Functional analysis of the chondroitin 6-sulfotransferase gene in relation to lymphocyte subpopulations, brain development, and oversulfated chondroitin sulfates. The Journal of Biological Chemistry 277: 1443–1450. doi: 10.1074/jbc.m104719200
[28]  Bashey RI, Sampson PM, Jimenez SA, Heimer R (1993) Glycosaminoglycans and chondroitin/dermatan sulfate proteoglycans in the myocardium of a non-human primate. Matrix 13: 363–371. doi: 10.1016/s0934-8832(11)80041-7
[29]  Hinek A, Teitell MA, Schoyer L, Allen W, Gripp KW, et al. (2005) Myocardial storage of chondroitin sulfate-containing moieties in Costello syndrome patients with severe hypertrophic cardiomyopathy. American Journal of Medical Genetics Part A 133A: 1–12. doi: 10.1002/ajmg.a.30495
[30]  Behrens J (2005) The role of the Wnt signalling pathway in colorectal tumorigenesis. Biochem Soc Trans 33: 672–675. doi: 10.1042/bst0330672
[31]  Cadigan KM, Peifer M (2009) Wnt signaling from development to disease: insights from model systems. Cold Spring Harb Perspect Biol 1: a002881. doi: 10.1101/cshperspect.a002881
[32]  Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469–480. doi: 10.1016/j.cell.2006.10.018
[33]  Fodde R, Brabletz T (2007) Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19: 150–158. doi: 10.1016/j.ceb.2007.02.007
[34]  Moon RT (2005) Wnt/beta-catenin pathway. Sci STKE 2005: cm1. doi: 10.1126/stke.2712005cm1
[35]  Nusse R (2005) Wnt signaling in disease and in development. Cell Res 15: 28–32. doi: 10.1038/sj.cr.7290260
[36]  Polakis P (2007) The many ways of Wnt in cancer. Curr Opin Genet Dev 17: 45–51. doi: 10.1016/j.gde.2006.12.007
[37]  Reya T, Clevers H (2005) Wnt signalling in stem cells and cancer. Nature 434: 843–850. doi: 10.1038/nature03319
[38]  Fevr T, Robine S, Louvard D, Huelsken J (2007) Wnt/beta-catenin is essential for intestinal homeostasis and maintenance of intestinal stem cells. Mol Cell Biol 27: 7551–7559. doi: 10.1128/mcb.01034-07
[39]  Gaspar C, Fodde R (2004) APC dosage effects in tumorigenesis and stem cell differentiation. Int J Dev Biol 48: 377–386. doi: 10.1387/ijdb.041807cg
[40]  Huelsken J, Held W (2009) Canonical Wnt signaling plays essential roles. Eur J Immunol 39: 3582–3583; author reply 3583–3584.
[41]  Nusse R, Fuerer C, Ching W, Harnish K, Logan C, et al. (2008) Wnt signaling and stem cell control. Cold Spring Harb Symp Quant Biol 73: 59–66. doi: 10.1101/sqb.2008.73.035
[42]  Hirata A, Utikal J, Yamashita S, Aoki H, Watanabe A, et al. (2013) Dose-dependent roles for canonical Wnt signalling in de novo crypt formation and cell cycle properties of the colonic epithelium. Development 140: 66–75. doi: 10.1242/dev.084103
[43]  Kühl SJ, Kühl M (2013) On the role of Wnt/beta-catenin signaling in stem cells. Biochimica et biophysica acta 1830: 2297–2306. doi: 10.1016/j.bbagen.2012.08.010
[44]  Ueno S, Weidinger G, Osugi T, Kohn AD, Golob JL, et al. (2007) Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proceedings of the National Academy of Sciences of the United States of America 104: 9685–9690. doi: 10.1073/pnas.0702859104
[45]  Gessert S, Kühl M (2010) The multiple phases and faces of wnt signaling during cardiac differentiation and development. Circulation Research 107: 186–199. doi: 10.1161/circresaha.110.221531
[46]  Kwon C, Cordes KR, Srivastava D (2008) Wnt/beta-catenin signaling acts at multiple developmental stages to promote mammalian cardiogenesis. Cell cycle 7: 3815–3818. doi: 10.4161/cc.7.24.7189
[47]  Nadanaka S, Ishida M, Ikegami M, Kitagawa H (2008) Chondroitin 4-O-sulfotransferase-1 modulates Wnt-3a signaling through control of E disaccharide expression of chondroitin sulfate. J Biol Chem 283: 27333–27343. doi: 10.1074/jbc.m802997200
[48]  Klüppel M (2011) Efficient secretion of biologically active Chondroitinase ABC from mammalian cells in the absence of an N-terminal signal peptide. Mol Cell Biochem 351: 1–11. doi: 10.1007/s11010-010-0705-1
[49]  Molenaar M, van de Wetering M, Oosterwegel M, Peterson-Maduro J, Godsave S, et al. (1996) XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell 86: 391–399. doi: 10.1016/s0092-8674(00)80112-9
[50]  Nagy A, Gertsenstein M, Vintersten K, Behringer R (2006) Differentiating Embryonic Stem (ES) Cells into Embryoid Bodies. CSH protocols 2006.
[51]  Dell’Era P, Ronca R, Coco L, Nicoli S, Metra M, et al. (2003) Fibroblast growth factor receptor-1 is essential for in vitro cardiomyocyte development. Circulation research 93: 414–420. doi: 10.1161/01.res.0000089460.12061.e1
[52]  Ronca R, Gualandi L, Crescini E, Calza S, Presta M, et al. (2009) Fibroblast growth factor receptor-1 phosphorylation requirement for cardiomyocyte differentiation in murine embryonic stem cells. Journal of Cellular and Molecular Medicine 13: 1489–1498. doi: 10.1111/j.1582-4934.2009.00805.x
[53]  Chen K, Wu L, Wang ZZ (2008) Extrinsic regulation of cardiomyocyte differentiation of embryonic stem cells. Journal of Cellular Biochemistry 104: 119–128. doi: 10.1002/jcb.21604
[54]  ten Dam GB, van de Westerlo EM, Purushothaman A, Stan RV, Bulten J, et al. (2007) Antibody GD3G7 selected against embryonic glycosaminoglycans defines chondroitin sulfate-E domains highly up-regulated in ovarian cancer and involved in vascular endothelial growth factor binding. The American Journal of Pathology 171: 1324–1333. doi: 10.2353/ajpath.2007.070111
[55]  Purushothaman A, Fukuda J, Mizumoto S, ten Dam GB, van Kuppevelt TH, et al. (2007) Functions of chondroitin sulfate/dermatan sulfate chains in brain development. Critical roles of E and iE disaccharide units recognized by a single chain antibody GD3G7. The Journal of Biological Chemistry 282: 19442–19452. doi: 10.1074/jbc.m700630200
[56]  Smetsers TF, van de Westerlo EM, ten Dam GB, Overes IM, Schalkwijk J, et al. (2004) Human single-chain antibodies reactive with native chondroitin sulfate detect chondroitin sulfate alterations in melanoma and psoriasis. The Journal of Investigative Dermatology 122: 707–716. doi: 10.1111/j.0022-202x.2004.22316.x
[57]  Peal DS, Burns CG, Macrae CA, Milan D (2009) Chondroitin sulfate expression is required for cardiac atrioventricular canal formation. Developmental dynamics : an official publication of the American Association of Anatomists 238: 3103–3110. doi: 10.1002/dvdy.22154
[58]  Hwang JY, Johnson PY, Braun KR, Hinek A, Fischer JW, et al. (2008) Retrovirally mediated overexpression of glycosaminoglycan-deficient biglycan in arterial smooth muscle cells induces tropoelastin synthesis and elastic fiber formation in vitro and in neointimae after vascular injury. The American Journal of Pathology 173: 1919–1928. doi: 10.2353/ajpath.2008.070875
[59]  Heegaard AM, Corsi A, Danielsen CC, Nielsen KL, Jorgensen HL, et al. (2007) Biglycan deficiency causes spontaneous aortic dissection and rupture in mice. Circulation 115: 2731–2738. doi: 10.1161/circulationaha.106.653980
[60]  Westermann D, Mersmann J, Melchior A, Freudenberger T, Petrik C, et al. (2008) Biglycan is required for adaptive remodeling after myocardial infarction. Circulation 117: 1269–1276. doi: 10.1161/circulationaha.107.714147
[61]  Gardner RT, Habecker BA (2013) Infarct-derived chondroitin sulfate proteoglycans prevent sympathetic reinnervation after cardiac ischemia-reperfusion injury. The Journal of neuroscience : the official journal of the Society for Neuroscience 33: 7175–7183. doi: 10.1523/jneurosci.5866-12.2013
[62]  Lam AP, Gottardi CJ (2011) beta-catenin signaling: a novel mediator of fibrosis and potential therapeutic target. Current opinion in rheumatology 23: 562–567. doi: 10.1097/bor.0b013e32834b3309
[63]  Oerlemans MI, Goumans MJ, van Middelaar B, Clevers H, Doevendans PA, et al. (2010) Active Wnt signaling in response to cardiac injury. Basic Res Cardiol 105: 631–641. doi: 10.1007/s00395-010-0100-9
[64]  Barker N, Clevers H (2006) Mining the Wnt pathway for cancer therapeutics. Nat Rev Drug Discov 5: 997–1014. doi: 10.1038/nrd2154
[65]  Prosperi JR, Goss KH (2010) A Wnt-ow of opportunity: targeting the Wnt/beta-catenin pathway in breast cancer. Curr Drug Targets 11: 1074–1088. doi: 10.2174/138945010792006780
[66]  Takahashi-Yanaga F, Kahn M (2010) Targeting Wnt signaling: can we safely eradicate cancer stem cells? Clin Cancer Res 16: 3153–3162. doi: 10.1158/1078-0432.ccr-09-2943
[67]  van Es JH, Clevers H (2005) Notch and Wnt inhibitors as potential new drugs for intestinal neoplastic disease. Trends Mol Med 11: 496–502. doi: 10.1016/j.molmed.2005.09.008

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