Extracellular matrix modulates the biological effects of melatonin in mesenchymal stem cells

Journal of Endocrinology

Volumn 223, Issue 2, 2014, Pages 167-180

  He, Fan ^a,b,c   Liu, Xiaozhen ^a   Xiong, Ke ^d   Chen, Sijin ^d   Zhou, Long ^b,c   Cui, Wenguo ^b,c   Pan, Guoqing ^b,c   Luo, Zong Ping ^b,c   Pei, Ming ^e   Gong, Yihong ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SOOCHOW UNIVERSITY   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^d SOUTHERN MEDICAL UNIVERSITY   (China)

^e WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Decellularized extracellular matrix; Melatonin; Mesenchymal stem cells; Superoxide dismutase

Indexed keywords

MELATONIN; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE;

ADSORPTION; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; CELL PROLIFERATION; DOWN REGULATION; ENZYME ASSAY; EXTRACELLULAR MATRIX; HORMONAL REGULATION; HUMAN; HUMAN CELL; MESENCHYMAL STEM CELL; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PROTEIN EXPRESSION; ABSORPTION; BONE DEVELOPMENT; CELL CULTURE; CULTURE TECHNIQUE; DRUG EFFECTS; MESENCHYMAL STROMA CELL; METABOLISM; OSTEOBLAST; PHYSIOLOGY; ULTRASTRUCTURE;

ABSORPTION, PHYSICOCHEMICAL; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; EXTRACELLULAR MATRIX; HUMANS; MELATONIN; MESENCHYMAL STROMAL CELLS; OSTEOBLASTS; OSTEOGENESIS; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE;

EID: 84915805900     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0430     Document Type: Article

References (51)

1. Alvarez-García V, González A, Alonso-González C, Martínez-Campa C & Cos S 2013 Antiangiogenic effects of melatonin in endothelial cell cultures. Microvascular Research 87 25-33. (doi:10.1016/j.mvr.2013. 02.008)
2. Cip1 expression. Journal of Biological Chemistry 277 13761-13770. (doi:10.1074/jbc.M111123200)
3. Bhat A, Boyadjiev SA, Senders CW & Leach JK 2011 Differential growth factor adsorption to calvarial osteoblast-secreted extracellular matrices instructs osteoblastic behavior. PLoS ONE 6 e25990. (doi:10.1371/ journal.pone.0025990)
4. Cardinali DP, Ladizesky MG, Boggio V, Cutrera RA & Mautalen C 2003 Melatonin effects on bone: experimental facts and clinical perspectives. Journal of Pineal Research 34 81-87. (doi:10.1034/j.1600-079X.2003. 00028.x)
5. Chen XD 2010 Extracellular matrix provides an optimal niche for the maintenance and propagation of mesenchymal stem cells. Birth Defects Research. Part C, Embryo Today: Reviews 90 45-54. (doi:10.1002/bdrc. 20171)
6. Chen XD, Dusevich V, Feng JQ, Manolagas SC & Jilka RL 2007 Extracellular matrix made by bone marrow cells facilitates expansion of marrow-derived mesenchymal progenitor cells and prevents their differentiation into osteoblasts. Journal of Bone and Mineral Research 22 1943-1956. (doi:10.1359/jbmr.070725)
7. Dumay A, Rincheval V, Trotot P, Mignotte B & Vayssiere JL 2006 The superoxide dismutase inhibitor diethyldithiocarbamate has antagonistic effects on apoptosis by triggering both cytochrome c release and caspase inhibition. Free Radical Biology & Medicine 40 1377-1390. (doi:10.1016/j.freeradbiomed.2005.12.005)
8. Feng YF, Wang L, Zhang Y, Li X, Ma ZS, Zou JW, Lei W & Zhang ZY 2013 Effect of reactive oxygen species overproduction on osteogenesis of porous titanium implant in the present of diabetes mellitus. Biomaterials 34 2234-2243. (doi:10.1016/j.biomaterials.2012.12.023)
9. Franceschi RT & Xiao G 2003 Regulation of the osteoblast-specific transcription factor, Runx2: responsiveness to multiple signal transduction pathways. Journal of Cellular Biochemistry 88 446-454. (doi:10.1002/jcb.10369)
10. Galasso O, Familiari F, De Gori M & Gasparini G 2012 Recent findings on the role of gelatinases (matrix metalloproteinase-2 and -9) in osteoarthritis. Advances in Orthopedics 2012 834208. (doi:10.1155/ 2012/834208)
11. Hamilton R & Campbell FR 1991 Immunochemical localization of extracellular materials in bone marrow of rats. Anatomical Record 231 218-224. (doi:10.1002/ar.1092310210)
12. Hayami T, Kapila YL & Kapila S 2011 Divergent upstream osteogenic events contribute to the differential modulation of MG63 cell osteoblast differentiation by MMP-1 (collagenase-1) and MMP-13 (collagenase-3). Matrix Biology 30 281-289. (doi:10.1016/j.matbio.2011.04.003)
13. He F & Pei M 2012 Rejuvenation of nucleus pulposus cells using extracellular matrix deposited by synovium-derived stem cells. Spine 37 459-469. (doi:10.1097/BRS.0b013e31821fcc64)
14. He F & Pei M 2013 Extracellular matrix enhances differentiation of adipose stem cells from infrapatellar fat pad toward chondrogenesis. Journal of Tissue Engineering and Regenerative Medicine 7 73-84. (doi:10.1002/term.505)
15. He F, Chen X & Pei M 2009 Reconstruction of an in vitro tissue-specific microenvironment to rejuvenate synovium-derived stem cells for cartilage tissue engineering. Tissue Engineering. Part A 15 3809-3821. (doi:10.1089/ten.tea.2009.0188)
16. He H, Liu X, Peng L, Gao Z, Ye Y, Su Y, Zhao Q, Wang K, Gong Y & He F 2013 Promotion of hepatic differentiation of bone marrow mesenchymal stem cells on decellularized cell-deposited extracellular matrix. BioMed Research International 2013 406871. (doi:10.1155/2013/406871)
17. Hempel U, Hintze V, Moller S, Schnabelrauch M, Scharnweber D & Dieter P 2012 Artificial extracellular matrices composed of collagen I and sulfated hyaluronan with adsorbed transforming growth factor b1 promote collagen synthesis of human mesenchymal stromal cells. Acta Biomaterialia 8 659-666. (doi:10.1016/j.actbio.2011.10.026)
18. Histing T, Anton C, Scheuer C, Garcia P, Holstein JH, Klein M, Matthys R, Pohlemann T & Menger MD 2012 Melatonin impairs fracture healing by suppressing RANKL-mediated bone remodeling. Journal of Surgical Research 173 83-90. (doi:10.1016/j.jss.2010.08.036)
19. Hu HM, Yang L, Wang Z, Liu YW, Fan JZ, Fan J, Liu J & Luo ZJ 2013 Overexpression of integrin a2 promotes osteogenic differentiation of hBMSCs from senile osteoporosis through the ERK pathway. International Journal of Clinical and Experimental Pathology 6 841-852.
20. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M et al. 2002 Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418 41-49. (doi:10.1038/nature00870)
21. Kim KJ, Choi JS, Kang I, Kim KW, Jeong CH & Jeong JW 2013 Melatonin suppresses tumor progression by reducing angiogenesis stimulated by HIF-1 in a mouse tumor model. Journal of Pineal Research 54 264-270. (doi:10.1111/j.1600-079X.2012.01030.x)
22. Kotlarczyk MP, Lassila HC, O'Neil CK, D'Amico F, Enderby LT, Witt-Enderby PA & Balk JL 2012 Melatonin osteoporosis prevention study (MOPS): a randomized, double-blind, placebo-controlled study examining the effects of melatonin on bone health and quality of life in perimenopausal women. Journal of Pineal Research 52 414-426. (doi:10.1111/j.1600-079X.2011.00956.x)
23. Koyama H, Nakade O, Takada Y, Kaku T & Lau KH 2002 Melatonin at pharmacologic doses increases bone mass by suppressing resorption through down-regulation of the RANKL-mediated osteoclast formation and activation. Journal of Bone and Mineral Research 17 1219-1229. (doi:10.1359/jbmr.2002.17.7.1219)
24. Lee NK, Choi YG, Baik JY, Han SY, Jeong DW, Bae YS, Kim N & Lee SY 2005 A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 106 852-859. (doi:10.1182/blood-2004-09-3662)
25. Li J, Hansen KC, Zhang Y, Dong C, Dinu CZ, Dzieciatkowska M & Pei M 2014 Rejuvenation of chondrogenic potential in a young stem cell microenvironment. Biomaterials 35 642-653. (doi:10.1016/ j.biomaterials.2013.09.099)
26. Linsley C, Wu B & Tawil B 2013 The effect of fibrinogen, collagen type I, and fibronectin on mesenchymal stem cell growth and differentiation into osteoblasts. Tissue Engineering. Part A 19 1416-1423. (doi:10.1089/ ten.tea.2012.0523)
27. Liu X, Gong Y, Xiong K, Ye Y, Xiong Y, Zhuang Z, Luo Y, Jiang Q & He F 2013 Melatonin mediates protective effects on inflammatory response induced by interleukin-1b in human mesenchymal stem cells. Journal of Pineal Research 55 14-25. (doi:10.1111/jpi.12045)
28. Liu X, Xu Y, Chen S, Tan Z, Xiong K, Li Y, Ye Y, Luo ZP, He F & Gong Y 2014 Rescue of proinflammatory cytokine-inhibited chondrogenesis by the antiarthritic effect of melatonin in synovium mesenchymal stem cells via suppression of reactive oxygen species and matrix metalloproteinases. Free Radical Biology & Medicine 68 234-246. (doi:10.1016/ j.freeradbiomed.2013.12.012)
29. Lopez-Martinez F, Olivares Ponce PN, Guerra Rodriguez M & Martinez Pedraza R 2012 Melatonin: bone metabolism in oral cavity. International Journal of Dentistry 2012 628406. (doi:10.1155/2012/ 628406)
30. Luchetti F, Canonico B, Bartolini D, Arcangeletti M, Ciffolilli S, Murdolo G, Piroddi M, Papa S, Reiter RJ & Galli F 2014 Melatonin regulates mesenchymal stem cell differentiation: a review. Journal of Pineal Research 56 382-397. (doi:10.1111/jpi.12133)
31. Maehata Y, Takamizawa S, Ozawa S, Izukuri K, Kato Y, Sato S, Lee MC, Kimura A & Hata R 2007 Type III collagen is essential for growth acceleration of human osteoblastic cells by ascorbic acid 2-phosphate, a long-acting vitamin C derivative. Matrix Biology 26 371-381. (doi:10.1016/j.matbio.2007.01.005)
32. Park KH, Kang JW, Lee EM, Kim JS, Rhee YH, Kim M, Jeong SJ, Park YG & Kim SH 2011 Melatonin promotes osteoblastic differentiation through the BMP/ERK/Wnt signaling pathways. Journal of Pineal Research 51 187-194. (doi:10.1111/j.1600-079X.2011.00875.x)
33. Pei M & He F 2012 Extracellular matrix deposited by synovium-derived stem cells delays replicative senescent chondrocyte dedifferentiation and enhances redifferentiation. Journal of Cellular Physiology 227 2163-2174. (doi:10.1002/jcp.22950)
34. Pei M, He F, Wei L & Rawson A 2009 Melatonin enhances cartilage matrix synthesis by porcine articular chondrocytes. Journal of Pineal Research 46 181-187. (doi:10.1111/j.1600-079X.2008.00646.x)
35. Pei M, He F & Kish VL 2011 Expansion on extracellular matrix deposited by human bone marrow stromal cells facilitates stem cell proliferation and tissue-specific lineage potential. Tissue Engineering. Part A 17 3067-3076. (doi:10.1089/ten.tea.2011.0158)
36. Pietila M, Palomaki S, Lehtonen S, Ritamo I, Valmu L, Nystedt J, Laitinen S, Leskela HV, Sormunen R, Pesala J et al. 2012 Mitochondrial function and energy metabolism in umbilical cord blood- and bone marrowderived mesenchymal stem cells. Stem Cells and Development 21 575-588. (doi:10.1089/scd.2011.0023)
37. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S &Marshak DR 1999 Multilineage potential of adult human mesenchymal stem cells. Science 284 143-147. (doi:10.1126/science.284.5411.143)
38. Poeggeler B, Reiter RJ, Tan DX, Chen LD & Manchester LC 1993Melatonin, hydroxyl radical-mediated oxidative damage, and aging: a hypothesis. Journal of Pineal Research 14 151-168. (doi:10.1111/j.1600-079X.1993. tb00498.x)
39. Radio NM, Doctor JS & Witt-Enderby PA 2006 Melatonin enhances alkaline phosphatase activity in differentiating human adult mesenchymal stem cells grown in osteogenic medium via MT2 melatonin receptors and the MEK/ERK (1/2) signaling cascade. Journal of Pineal Research 40 332-342. (doi:10.1111/j.1600-079X.2006.00318.x)
40. Ramírez-Fernández MP, Calvo-Guirado JL, de-Val JE, Delgado-Ruiz RA, Negri B, Pardo-Zamora G, Peñarrocha D, Barona C, Granero JM & Alcaraz-Baños M 2013 Melatonin promotes angiogenesis during repair of bone defects: a radiological and histomorphometric study in rabbit tibiae. Clinical Oral Investigations 17 147-158. (doi:10.1007/ s00784-012-0684-6)
41. Sadr N, Pippenger BE, Scherberich A, Wendt D, Mantero S, Martin I & Papadimitropoulos A 2012 Enhancing the biological performance of synthetic polymeric materials by decoration with engineered, decellularized extracellular matrix. Biomaterials 33 5085-5093. (doi:10.1016/j.biomaterials.2012.03.082)
42. Sanchez-Barcelo EJ, Mediavilla MD, Tan DX & Reiter RJ 2010 Scientific basis for the potential use of melatonin in bone diseases: osteoporosis and adolescent idiopathic scoliosis. Journal of Osteoporosis 2010 830231. (doi:10.4061/2010/830231)
43. Sciancalepore M, Luin E, Parato G, Ren E, Giniatullin R, Fabbretti E & Lorenzon P 2012 Reactive oxygen species contribute to the promotion of the ATP-mediated proliferation of mouse skeletal myoblasts. Free Radical Biology &Medicine 53 1392-1398. (doi:10.1016/j.freeradbiomed. 2012.08.002)
44. Sethi S, Radio NM, Kotlarczyk MP, Chen CT, Wei YH, Jockers R & Witt-Enderby PA 2010 Determination of the minimal melatonin exposure required to induce osteoblast differentiation from human mesenchymal stem cells and these effects on downstream signaling pathways. Journal of Pineal Research 49 222-238. (doi:10.1111/ j.1600-079X.2010.00784.x)
45. Sun Y, Li W, Lu Z, Chen R, Ling J, Ran Q, Jilka RL & Chen XD 2011 Rescuing replication and osteogenesis of aged mesenchymal stem cells by exposure to a young extracellular matrix. FASEB Journal 25 1474-1485. (doi:10.1096/fj.10-161497)
46. Swarnakar S, Paul S, Singh LP & Reiter RJ 2011 Matrix metalloproteinases in health and disease: regulation by melatonin. Journal of Pineal Research 50 8-20. (doi:10.1111/j.1600-079X.2010.00812.x)
47. Tan DX, Manchester LC, Reiter RJ, Qi WB, Zhang M, Weintraub ST, Cabrera J, Sainz RM & Mayo JC 1999 Identification of highly elevated levels of melatonin in bone marrow: its origin and significance. Biochimica et Biophysica Acta 1472 206-214. (doi:10.1016/S0304-4165(99)00125-7)
48. Wang FS, Yang KD, Wang CJ, Huang HC, Chio CC, Hsu TY & Ou CY 2004 Shockwave stimulates oxygen radical-mediated osteogenesis of the mesenchymal cells from human umbilical cord blood. Journal of Bone and Mineral Research 19 973-982. (doi:10.1359/JBMR.040121)
49. Yamada Y, Tamura T, Hariu K, Asano Y, Sato S & Ito K 2008 Angiogenesis in newly augmented bone observed in rabbit calvarium using a titanium cap. Clinical Oral Implants Research 19 1003-1009. (doi:10.1111/j.1600-0501.2008.01554.x)
50. Zhang L, Su P, Xu C, Chen C, Liang A, Du K, Peng Y & Huang D 2010 Melatonin inhibits adipogenesis and enhances osteogenesis of human mesenchymal stem cells by suppressing PPARg expression and enhancing Runx2 expression. Journal of Pineal Research 49 364-372. (doi:10.1111/j.1600-079X.2010.00803.x)
51. Zhou X, Zhang Z, Feng JQ, Dusevich VM, Sinha K, Zhang H, Darnay BG & de Crombrugghe B 2010 Multiple functions of Osterix are required for bone growth and homeostasis in postnatal mice. PNAS 107 12919-12924. (doi:10.1073/pnas.0912855107)