Hyaluronan Is Crucial for Stem Cell Differentiation into Smooth Muscle Lineage

Stem Cells

Volumn 34, Issue 5, 2016, Pages 1225-1238

  Simpson, Russell M L ^a   Hong, Xuechong ^a   Wong, Mei Mei ^a   Karamariti, Eirini ^a   Bhaloo, Shirin Issa ^a   Warren, Derek ^a   Kong, Wei ^b   Hu, Yanhua ^a   Xu, Qingbo ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b PEKING UNIVERSITY   (China)

Author keywords

Hyaluronan; Neointima; Smooth muscle cells; Stem cells; Vasculogenesis

Indexed keywords

COLLAGEN TYPE 4; EPIDERMAL GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; HYALURONAN SYNTHASE 2; HYALURONIC ACID; HYALURONIDASE; HYMECROMONE; MATRIGEL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SYNTHETASE; UNCLASSIFIED DRUG; HYALURONATE SYNTHETASE; HYALURONIC ACID BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BINDING;

ADENOVIRIDAE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DIFFERENTIATION; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; EX VIVO STUDY; GENE OVEREXPRESSION; GENE SILENCING; GENE TRANSFER; HUMAN; HUMAN CELL; MOLECULAR WEIGHT; MOUSE; NEOINTIMA; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; SYNTHESIS; TISSUE ENGINEERING; VASCULAR TISSUE; VEIN GRAFT; ANIMAL; BIOLOGICAL MODEL; BIOSYNTHESIS; CELL LINEAGE; CYTOLOGY; ENZYME ACTIVATION; EXTRACELLULAR SPACE; MAPK SIGNALING; METABOLISM; MOUSE EMBRYONIC STEM CELL; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; EXTRACELLULAR SPACE; HYALURONAN RECEPTORS; HYALURONAN SYNTHASES; HYALURONIC ACID; MAP KINASE SIGNALING SYSTEM; MICE; MODELS, BIOLOGICAL; MOUSE EMBRYONIC STEM CELLS; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN BINDING; RECEPTOR, EPIDERMAL GROWTH FACTOR; UP-REGULATION;

EID: 84959558362     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.2328     Document Type: Article

References (60)

1. Evans MJ, Kaufman MH,. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981; 292: 154-156.
2. Martin GR,. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci USA 1981; 78: 7634-7638.
3. Sinha S, Hoofnagle MH, Kingston PA, et al., Transforming growth factor-beta1 signaling contributes to development of smooth muscle cells from embryonic stem cells. Am J Physiol Cell Physiol 2004; 287: C1560-1568.
4. Xiao Q, Zeng L, Zhang Z, et al., Stem cell-derived Sca-1 + progenitors differentiate into smooth muscle cells, which is mediated by collagen IV-integrin alpha1/beta1/alphav and PDGF receptor pathways. Am J Physiol Cell Physiol 2007; 292: C342-352.
5. Brizzi MF, Tarone G, Defilippi P,. Extracellular matrix, integrins, and growth factors as tailors of the stem cell niche. Curr Opin Cell Biol 2012; 24: 645-651.
6. Li X, Chu J, Wang A, et al., Uniaxial mechanical strain modulates the differentiation of neural crest stem cells into smooth muscle lineage on micropatterned surfaces. PloS one 2011; 6: e26029.
7. Watt FM, Huck WT,. Role of the extracellular matrix in regulating stem cell fate. Nat Rev Mol Cell Biol 2013; 14: 467-473.
8. Qu C, Rilla K, Tammi R, et al., Extensive CD44-dependent hyaluronan coats on human bone marrow-derived mesenchymal stem cells produced by hyaluronan synthases HAS1, HAS2 and HAS3. Int J Biochem Cell Biol 2014; 48: 45-54.
9. Choudhary M, Zhang X, Stojkovic P, et al., Putative role of hyaluronan and its related genes, HAS2 and RHAMM, in human early preimplantation embryogenesis and embryonic stem cell characterization. Stem Cells 2007; 25: 3045-3057.
10. Calabro A, Oken MM, Hascall VC, et al., Characterization of hyaluronan synthase expression and hyaluronan synthesis in bone marrow mesenchymal progenitor cells: Predominant expression of HAS1 mRNA and up-regulated hyaluronan synthesis in bone marrow cells derived from multiple myeloma patients. Blood 2002; 100: 2578-2585.
11. Nilsson SK, Haylock DN, Johnston HM, et al., Hyaluronan is synthesized by primitive hemopoietic cells, participates in their lodgment at the endosteum following transplantation, and is involved in the regulation of their proliferation and differentiation in vitro. Blood 2003; 101: 856-862.
12. Pilarski LM, Pruski E, Wizniak J, et al., Potential role for hyaluronan and the hyaluronan receptor RHAMM in mobilization and trafficking of hematopoietic progenitor cells. Blood 1999; 93: 2918-2927.
13. Chung C, Burdick JA,. Influence of three-dimensional hyaluronic acid microenvironments on mesenchymal stem cell chondrogenesis. Tissue Eng Part A 2009; 15: 243-254.
14. Spicer AP, McDonald JA,. Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family. J Biol Chem 1998; 273: 1923-1932.
15. Spicer AP, Kaback LA, Smith TJ, et al., Molecular cloning and characterization of the human and mouse UDP-glucose dehydrogenase genes. J Biol Chem 1998; 273: 25117-25124.
16. Shukla S, Nair R, Rolle MW, et al., Synthesis and organization of hyaluronan and versican by embryonic stem cells undergoing embryoid body differentiation. J Histochem Cytochem 2010; 58: 345-358.
17. Zoltan-Jones A, Huang L, Ghatak S, et al., Elevated hyaluronan production induces mesenchymal and transformed properties in epithelial cells. J Biol Chem 2003; 278: 45801-45810.
18. Simpson RM, Wells A, Thomas D, et al., Aging fibroblasts resist phenotypic maturation because of impaired hyaluronan-dependent CD44/epidermal growth factor receptor signaling. Am J Pathol 2010; 176: 1215-1228.
19. Simpson RM, Meran S, Thomas D, et al., Age-related changes in pericellular hyaluronan organization leads to impaired dermal fibroblast to myofibroblast differentiation. Am J Pathol 2009; 175: 1915-1928.
20. Chen PY, Huang LL, Hsieh HJ,. Hyaluronan preserves the proliferation and differentiation potentials of long-term cultured murine adipose-derived stromal cells. Biochem Biophys Res Commun 2007; 360: 1-6.
21. Itano N, Atsumi F, Sawai T, et al., Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. Proc Natl Acad Sci USA 2002; 99: 3609-3614.
22. Ito T, Williams JD, Al-Assaf S, et al., Hyaluronan and proximal tubular cell migration. Kidney Int 2004; 65: 823-833.
23. Legg JW, Lewis CA, Parsons M, et al., A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nat Cell Biol 2002; 4: 399-407.
24. Brecht M, Mayer U, Schlosser E, et al., Increased hyaluronate synthesis is required for fibroblast detachment and mitosis. Biochem J 1986; 239: 445-450.
25. Evanko SP, Angello JC, Wight TN,. Formation of hyaluronan- and versican-rich pericellular matrix is required for proliferation and migration of vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 1999; 19: 1004-1013.
26. Moyer KE, Ehrlich HP,. Modulation of human fibroblast gap junction intercellular communication by hyaluronan. J Cell Physiol 2003; 196: 165-170.
27. Cyphert JM, Trempus CS, Garantziotis S,. Size matters: Molecular weight specificity of hyaluronan effects in cell biology. Int J Cell Biol 2015; 2015: 563818.
28. Itano N, Sawai T, Atsumi F, et al., Selective expression and functional characteristics of three mammalian hyaluronan synthases in oncogenic malignant transformation. J Biol Chem 2004; 279: 18679-18687.
29. Itano N, Kimata K,. Mammalian hyaluronan synthases. IUBMB Life 2002; 54: 195-199.
30. Itano N, Sawai T, Yoshida M, et al., Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J Biol Chem 1999; 274: 25085-25092.
31. Spicer AP, Nguyen TK,. Mammalian hyaluronan synthases: Investigation of functional relationships in vivo. Biochem Soc Trans 1999; 27: 109-115.
32. Weigel PH, DeAngelis PL,. Hyaluronan synthases: A decade-plus of novel glycosyltransferases. J Biol Chem 2007; 282: 36777-36781.
33. Solis MA, Chen YH, Wong TY, et al., Hyaluronan regulates cell behavior: A potential niche matrix for stem cells. Biochem Res Int 2012; 2012: 346972.
34. Schraufstatter IU, Serobyan N, Loring J, et al., Hyaluronan is required for generation of hematopoietic cells during differentiation of human embryonic stem cells. J Stem Cells 2010; 5: 9-21.
35. Gerecht S, Burdick JA, Ferreira LS, et al., Hyaluronic acid hydrogel for controlled self-renewal and differentiation of human embryonic stem cells. Proc Natl Acad Sci USA 2007; 104: 11298-11303.
36. Ferreira LS, Gerecht S, Fuller J, et al., Bioactive hydrogel scaffolds for controllable vascular differentiation of human embryonic stem cells. Biomaterials 2007; 28: 2706-2717.
37. Peattie RA, Nayate AP, Firpo MA, et al., Stimulation of in vivo angiogenesis by cytokine-loaded hyaluronic acid hydrogel implants. Biomaterials 2004; 25: 2789-2798.
38. Lam J, Truong NF, Segura T,. Design of cell-matrix interactions in hyaluronic acid hydrogel scaffolds. Acta Biomater 2014; 10: 1571-1580.
39. Zou Y, Dietrich H, Hu Y, et al., Mouse model of venous bypass graft arteriosclerosis. Am J Pathol 1998; 153: 1301-1310.
40. Kakizaki I, Kojima K, Takagaki K, et al., A novel mechanism for the inhibition of hyaluronan biosynthesis by 4-methylumbelliferone. J Biol Chem 2004; 279: 33281-33289.
41. Bourguignon LY, Gilad E, Brightman A, et al., Hyaluronan-CD44 interaction with leukemia-associated RhoGEF and epidermal growth factor receptor promotes Rho/Ras co-activation, phospholipase C epsilon-Ca2 + signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. J Biol Chem 2006; 281: 14026-14040.
42. Kashima Y, Takahashi M, Shiba Y, et al., Crucial role of hyaluronan in neointimal formation after vascular injury. PloS one 2013; 8: e58760.
43. Meran S, Luo DD, Simpson R, et al., Hyaluronan facilitates transforming growth factor-beta1-dependent proliferation via CD44 and epidermal growth factor receptor interaction. J Biol Chem 2011; 286: 17618-17630.
44. Zeng L, Xiao Q, Margariti A, et al., HDAC3 is crucial in shear- and VEGF-induced stem cell differentiation toward endothelial cells. J Cell Biol 2006; 174: 1059-1069.
45. Liu CM, Chang CH, Yu CH, et al., Hyaluronan substratum induces multidrug resistance in human mesenchymal stem cells via CD44 signaling. Cell Tissue Res 2009; 336: 465-475.
46. Liu CM, Yu CH, Chang CH, et al., Hyaluronan substratum holds mesenchymal stem cells in slow-cycling mode by prolonging G1 phase. Cell Tissue Res 2008; 334: 435-443.
47. Clarkin CE, Allen S, Wheeler-Jones CP, et al., Reduced chondrogenic matrix accumulation by 4-methylumbelliferone reveals the potential for selective targeting of UDP-glucose dehydrogenase. Matrix Biol 2011; 30: 163-168.
48. Eggli PS, Graber W,. Association of hyaluronan with rat vascular endothelial and smooth muscle cells. J Histochem Cytochem 1995; 43: 689-697.
49. Bourguignon LY, Wong G, Earle C, et al., Hyaluronan-CD44 interaction promotes c-Src-mediated twist signaling, microRNA-10b expression, and RhoA/RhoC up-regulation, leading to Rho-kinase-associated cytoskeleton activation and breast tumor cell invasion. J Biol Chem 2010; 285: 36721-36735.
50. Bourguignon LY, Peyrollier K, Xia W, et al., Hyaluronan-CD44 interaction activates stem cell marker Nanog, Stat-3-mediated MDR1 gene expression, and ankyrin-regulated multidrug efflux in breast and ovarian tumor cells. J Biol Chem 2008; 283: 17635-17651.
51. Tammi R, Rilla K, Pienimaki JP, et al., Hyaluronan enters keratinocytes by a novel endocytic route for catabolism. J Biol Chem 2001; 276: 35111-35122.
52. Evanko SP, Wight TN,. Intracellular localization of hyaluronan in proliferating cells. J Histochem Cytochem 1999; 47: 1331-1342.
53. Marquez C, Trigueros C, Fernandez E, et al., The development of T and non-T cell lineages from CD34 + human thymic precursors can be traced by the differential expression of CD44. J Exp Med 1995; 181: 475-483.
54. Toole BP,. Hyaluronan: From extracellular glue to pericellular cue. Nat Rev Cancer 2004; 4: 528-539.
55. Keller KE, Sun YY, Vranka JA, et al., Inhibition of hyaluronan synthesis reduces versican and fibronectin levels in trabecular meshwork cells. PloS One 2012; 7: e48523.
56. Abhold EL, Kiang A, Rahimy E, et al., EGFR kinase promotes acquisition of stem cell-like properties: A potential therapeutic target in head and neck squamous cell carcinoma stem cells. PloS one 2012; 7: e32459.
57. Burdon T, Stracey C, Chambers I, et al., Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev Biol 1999; 210: 30-43.
58. Pasonen-Seppanen SM, Maytin EV, Torronen KJ, et al., All-trans retinoic acid-induced hyaluronan production and hyperplasia are partly mediated by EGFR signaling in epidermal keratinocytes. J Invest Dermatol 2008; 128: 797-807.
59. Tang Z, Wang A, Yuan F, et al., Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat Commun 2012; 3: 875.
60. Chen Y, Wong MM, Campagnolo P, et al., Adventitial stem cells in vein grafts display multilineage potential that contributes to neointimal formation. Arterioscler Thromb Vasc Biol 2013; 33: 1844-1851.