Open Access

Comparison of adipose‑ and bone marrow‑derived stem cells in protecting against ox‑LDL‑induced inflammation in M1‑macrophage‑derived foam cells

  • Authors:
    • Jian‑Zhong Li
    • Tian‑Hui Cao
    • Jin‑Cheng Han
    • Hui Qu
    • Shuang‑Quan Jiang
    • Bao‑Dong Xie
    • Xiao‑Long Yan
    • Hua Wu
    • Xiang‑Lan Liu
    • Fan Zhang
    • Xiao‑Ping Leng
    • Kai Kang
    • Shu‑Lin Jiang
  • View Affiliations

  • Published online on: February 1, 2019     https://doi.org/10.3892/mmr.2019.9922
  • Pages: 2660-2670
  • Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Adipose‑derived stem cells (ADSCs) and bone marrow‑derived stem cells (BMSCs) are considered to be prospective sources of mesenchymal stromal cells (MSCs), that can be used in cell therapy for atherosclerosis. The present study investigated whether ADSCs co‑cultured with M1 foam macrophages via treatment with oxidized low‑density lipoprotein (ox‑LDL) would lead to similar or improved anti‑inflammatory effects compared with BMSCs. ADSCs, peripheral blood monocytes, BMSCs and ox‑LDL were isolated from ten coronary heart disease (CHD) patients. After three passages, the supernatants of the ADSCs and BMSCs were collected and systematically analysed by liquid chromatography‑quadrupole time‑of‑flight‑mass spectrometry (6530; Agilent Technologies, Inc., Santa Clara, CA, USA). Cis‑9, trans‑11 was deemed to be responsible for the potential differences in the metabolic characteristics of ADSCs and BMSCs. These peripheral blood monocytes were characterized using flow cytometry. Following peripheral blood monocytes differentiation into M1 macrophages, the formation of M1 foam macrophages was achieved through treatment with ox‑LDL. Overall, 2x106 ADSCs, BMSCs or BMSCs+cis‑9, trans‑11 were co‑cultured with M1 foam macrophages. Anti‑inflammatory capability, phagocytic activity, anti‑apoptotic capability and cell viability assays were compared among these groups. It was demonstrated that the accumulation of lipid droplets decreased following ADSCs, BMSCs or BMSCs+cis‑9, trans‑11 treatment in M1 macrophages derived from foam cells. Consistently, ADSCs exhibited great advantageous anti‑inflammatory capabilities, phagocytic activity, anti‑apoptotic capability activity and cell viability over BMSCs or BMSCs+cis‑9, trans‑11. Additionally, BMSCs+cis‑9, trans‑11 also demonstrated marked improvement in anti‑inflammatory capability, phagocytic activity, anti‑apoptotic capability activity and cell viability in comparison with BMSCs. The present results indicated that ADSCs would be more appropriate for transplantation to treat atherosclerosis than BMSCs alone or BMSCs+cis‑9, trans‑11. This may be an important mechanism to regulate macrophage immune function.

References

1 

Cheong C and Choi JH: Dendritic cells and regulatory T cells in atherosclerosis. Mol Cells. 34:341–347. 2012. View Article : Google Scholar : PubMed/NCBI

2 

Frostegård J: Immunity, atherosclerosis and cardiovascular disease. BMC Med. 11:1172013. View Article : Google Scholar : PubMed/NCBI

3 

Gerry AB and Leake DS: Effect of low extracellular pH on NF-κB activation in macrophages. Atherosclerosis. 233:537–544. 2014. View Article : Google Scholar : PubMed/NCBI

4 

Wigren M, Nilsson J and Kolbus D: Lymphocytes in atherosclerosis. Clin Chim Acta. 413:1562–1568. 2012. View Article : Google Scholar : PubMed/NCBI

5 

Callegari A, Coons ML, Ricks JL, Yang HL, Gross TS, Huber P, Rosenfeld ME and Scatena M: Bone marrow- or vessel wall-derived osteoprotegerin is sufficient to reduce atherosclerotic lesion size and vascular calcification. Arterioscler Thromb Vasc Biol. 33:2491–2500. 2013. View Article : Google Scholar : PubMed/NCBI

6 

Eirin A, Zhu XY, Krier JD, Tang H, Jordan KL, Grande JP, Lerman A, Textor SC and Lerman LO: Adipose tissue-derived mesenchymal stem cells improve revascularization outcomes to restore renal function in swine atherosclerotic renal artery stenosis. Stem Cells. 30:1030–1041. 2012. View Article : Google Scholar : PubMed/NCBI

7 

Yoon YS, Wecker A, Heyd L, Park JS, Tkebuchava T, Kusano K, Hanley A, Scadova H, Qin G, Cha DH, et al: Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest. 115:326–338. 2005. View Article : Google Scholar : PubMed/NCBI

8 

Gojo S, Gojo N, Takeda Y, Mori T, Abe H, Kyo S, Hata J and Umezawa A: In vivo cardiovasculogenesis by direct injection of isolated adult mesenchymal stem cells. Exp Cell Res. 288:51–59. 2003. View Article : Google Scholar : PubMed/NCBI

9 

Ichim TE, Alexandrescu DT, Solano F, Lara F, Campion Rde N, Paris E, Woods EJ, Murphy MP, Dasanu CA, Patel AN, et al: Mesenchymal stem cells as anti-inflammatories: Implications for treatment of Duchenne muscular dystrophy. Cell Immunol. 260:75–82. 2010. View Article : Google Scholar : PubMed/NCBI

10 

Sharma AK, Bury MI, Fuller NJ, Marks AJ, Kollhoff DM, Rao MV, Hota PV, Matoka DJ, Edassery SL, Thaker H, et al: Cotransplantation with specific populations of spina bifida bone marrow stem/progenitor cells enhances urinary bladder regeneration. Proc Natl Acad Sci USA. 110:4003–4008. 2013. View Article : Google Scholar : PubMed/NCBI

11 

Sharma AK, Hota PV, Matoka DJ, Fuller NJ, Jandali D, Thaker H, Ameer GA and Cheng EY: Urinary bladder smooth muscle regeneration utilizing bone marrow derived mesenchymal stem cell seeded elastomeric poly(1,8-octanediol-co-citrate) based thin films. Biomaterials. 31:6207–6217. 2010. View Article : Google Scholar : PubMed/NCBI

12 

Anderson P, Souza-Moreira L, Morell M, Caro M, O'Valle F, Gonzalez-Rey E and Delgado M: Adipose-derived mesenchymal stromal cells induce immunomodulatory macrophages which protect from experimental colitis and sepsis. Gut. 62:1131–1141. 2013. View Article : Google Scholar : PubMed/NCBI

13 

Wise AF, Williams TM, Kiewiet MB, Payne NL, Siatskas C, Samuel CS and Ricardo SD: Human mesenchymal stem cells alter macrophage phenotype and promote regeneration via homing to the kidney following ischemia-reperfusion injury. Am J Physiol Renal Physiol. 306:F1222–F1235. 2014. View Article : Google Scholar : PubMed/NCBI

14 

Heneidi S, Simerman AA, Keller E, Singh P, Li X, Dumesic DA and Chazenbalk G: Awakened by cellular stress: Isolation and characterization of a novel population of pluripotent stem cells derived from human adipose tissue. PLoS One. 8:e647522013. View Article : Google Scholar : PubMed/NCBI

15 

Russo V, Yu C, Belliveau P, Hamilton A and Flynn LE: Comparison of human adipose-derived stem cells isolated from subcutaneous, omental, and intrathoracic adipose tissue depots for regenerative applications. Stem Cells Transl Med. 3:206–217. 2014. View Article : Google Scholar : PubMed/NCBI

16 

Kang K, Sun L, Xiao Y, Li SH, Wu J, Guo J, Jiang SL, Yang L, Yau TM, Weisel RD, et al: Aged human cells rejuvenated by cytokine enhancement of biomaterials for surgical ventricular restoration. J Am Coll Cardiol. 60:2237–2249. 2012. View Article : Google Scholar : PubMed/NCBI

17 

Müller I, Schönberger T, Schneider M, Borst O, Ziegler M, Seizer P, Leder C, Müller K, Lang M, Appenzeller F, et al: Gremlin-1 is an inhibitor of macrophage migration inhibitory factor and attenuates atherosclerotic plaque growth in ApoE-/-mice. J Biol Chem. 288:31635–31645. 2013. View Article : Google Scholar : PubMed/NCBI

18 

Seizer P, Schönberger T, Schött M, Lang MR, Langer HF, Bigalke B, Krämer BF, Borst O, Daub K, Heidenreich O, et al: EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation. Atherosclerosis. 209:51–57. 2010. View Article : Google Scholar : PubMed/NCBI

19 

Boullier A, Li Y, Quehenberger O, Palinski W, Tabas I, Witztum JL and Miller YI: Minimally oxidized LDL offsets the apoptotic effects of extensively oxidized LDL and free cholesterol in macrophages. Arterioscler Thromb Vasc Biol. 26:1169–1176. 2006. View Article : Google Scholar : PubMed/NCBI

20 

Yao S, Sang H, Song G, Yang N, Liu Q, Zhang Y, Jiao P, Zong C and Qin S: Quercetin protects macrophages from oxidized low-density lipoprotein-induced apoptosis by inhibiting the endoplasmic reticulum stress-C/EBP homologous protein pathway. Exp Biol Med (Maywood). 237:822–831. 2012. View Article : Google Scholar : PubMed/NCBI

21 

Hong L, Xie ZZ, Du YH, Tang YB, Tao J, Lv XF, Zhou JG and Guan YY: Alteration of volume-regulated chloride channel during macrophage-derived foam cell formation in atherosclerosis. Atherosclerosis. 216:59–66. 2011. View Article : Google Scholar : PubMed/NCBI

22 

Ricci R, Sumara G, Sumara I, Rozenberg I, Kurrer M, Akhmedov A, Hersberger M, Eriksson U, Eberli FR, Becher B, et al: Requirement of JNK2 for scavenger receptor A-mediated foam cell formation in atherogenesis. Science. 306:1558–1561. 2004. View Article : Google Scholar : PubMed/NCBI

23 

Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI

24 

Ayaori M, Sawada S, Yonemura A, Iwamoto N, Ogura M, Tanaka N, Nakaya K, Kusuhara M, Nakamura H and Ohsuzu F: Glucocorticoid receptor regulates ATP-binding cassette transporter-A1 expression and apolipoprotein-mediated cholesterol efflux from macrophages. Arterioscler Thromb Vasc Biol. 26:163–168. 2006. View Article : Google Scholar : PubMed/NCBI

25 

Trygg J, Holmes E and Lundstedt T: Chemometrics in metabonomics. J Proteome Res. 6:469–479. 2007. View Article : Google Scholar : PubMed/NCBI

26 

van Velzen EJ, Westerhuis JA, van Duynhoven JP, van Dorsten FA, Hoefsloot HC, Jacobs DM, Smit S, Draijer R, Kroner CI and Smilde AK: Multilevel data analysis of a crossover designed human nutritional intervention study. J Proteome Res. 7:4483–4491. 2008. View Article : Google Scholar : PubMed/NCBI

27 

Ross R: Rous-whipple award lecture. Atherosclerosis: A defense mechanism gone awry. Am J Pathol. 143:987–1002. 1993.PubMed/NCBI

28 

Pennings M, Meurs I, Ye D, Out R, Hoekstra M, Van Berkel TJ and Van Eck M: Regulation of cholesterol homeostasis in macrophages and consequences for atherosclerotic lesion development. FEBS Lett. 580:5588–5596. 2006. View Article : Google Scholar : PubMed/NCBI

29 

Kritchevsky D, Tepper SA, Wright S, Czarnecki SK, Wilson TA and Nicolosi RJ: Conjugated linoleic acid isomer effects in atherosclerosis: Growth and regression of lesions. Lipids. 39:611–616. 2004. View Article : Google Scholar : PubMed/NCBI

30 

Lee KN, Kritchevsky D and Pariza MW: Conjugated linoleic acid and atherosclerosis in rabbits. Atherosclerosis. 108:19–25. 1994. View Article : Google Scholar : PubMed/NCBI

31 

Toomey S, Harhen B, Roche HM, Fitzgerald D and Belton O: Profound resolution of early atherosclerosis with conjugated linoleic acid. Atherosclerosis. 187:40–49. 2006. View Article : Google Scholar : PubMed/NCBI

32 

Arbonés-Mainar JM, Navarro MA, Guzmán MA, Arnal C, Surra JC, Acín S, Carnicer R, Osada J and Roche HM: Selective effect of conjugated linoleic acid isomers on atherosclerotic lesion development in apolipoprotein E knockout mice. Atherosclerosis. 189:318–327. 2006. View Article : Google Scholar : PubMed/NCBI

33 

Ramakers JD, Plat J, Sébédio JL and Mensink RP: Effects of the individual isomers cis-9,trans-11 vs. trans-10,cis-12 of conjugated linoleic acid (CLA) on inflammation parameters in moderately overweight subjects with LDL-phenotype B. Lipids. 40:909–918. 2005. View Article : Google Scholar : PubMed/NCBI

34 

Schleser S, Ringseis R and Eder K: Conjugated linoleic acids have no effect on TNF alpha-induced adhesion molecule expression, U937 monocyte adhesion, and chemokine release in human aortic endothelial cells. Atherosclerosis. 186:337–344. 2006. View Article : Google Scholar : PubMed/NCBI

35 

Zhang H, Guo Y and Yuan J: Conjugated linoleic acid enhanced the immune function in broiler chicks. Br J Nutr. 94:746–752. 2005. View Article : Google Scholar : PubMed/NCBI

36 

Dayan V, Yannarelli G, Billia F, Filomeno P, Wang XH, Davies JE and Keating A: Mesenchymal stromal cells mediate a switch to alternatively activated monocytes/macrophages after acute myocardial infarction. Basic Res Cardiol. 106:1299–1310. 2011. View Article : Google Scholar : PubMed/NCBI

37 

Kim J and Hematti P: Mesenchymal stem cell-educated macrophages: A novel type of alternatively activated macrophages. Exp Hematol. 37:1445–1453. 2009. View Article : Google Scholar : PubMed/NCBI

38 

Németh K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, et al: Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med. 15:42–49. 2009. View Article : Google Scholar : PubMed/NCBI

39 

Adutler-Lieber S, Ben-Mordechai T, Naftali-Shani N, Asher E, Loberman D, Raanani E and Leor J: Human macrophage regulation via interaction with cardiac adipose tissue-derived mesenchymal stromal cells. J Cardiovasc Pharmacol Ther. 18:78–86. 2013. View Article : Google Scholar : PubMed/NCBI

40 

Stachowska E, Baśkiewicz-Masiuk M, Dziedziejko V, Adler G, Bober J, Machaliński B and Chlubek D: Conjugated linoleic acids can change phagocytosis of human monocytes/macrophages by reduction in Cox-2 expression. Lipids. 42:707–716. 2007. View Article : Google Scholar : PubMed/NCBI

41 

Jiang D, Qi Y, Walker NG, Sindrilaru A, Hainzl A, Wlaschek M, MacNeil S and Scharffetter-Kochanek K: The effect of adipose tissue derived MSCs delivered by a chemically defined carrier on full-thickness cutaneous wound healing. Biomaterials. 34:2501–2515. 2013. View Article : Google Scholar : PubMed/NCBI

42 

Lee Y, Thompson JT and Vanden Heuvel JP: 9E,11E-conjugated linoleic acid increases expression of the endogenous antiinflammatory factor, interleukin-1 receptor antagonist, in RAW 264.7 cells. J Nutr. 139:1861–1866. 2009. View Article : Google Scholar : PubMed/NCBI

43 

Yu Y, Correll PH and Vanden Heuvel JP: Conjugated linoleic acid decreases production of pro-inflammatory products in macrophages: Evidence for a PPAR gamma-dependent mechanism. Biochim Biophys Acta. 1581:89–99. 2002. View Article : Google Scholar : PubMed/NCBI

44 

Wang Y, Wang GZ, Rabinovitch PS and Tabas I: Macrophage mitochondrial oxidative stress promotes atherosclerosis and nuclear factor-κB-mediated inflammation in macrophages. Circ Res. 114:421–433. 2014. View Article : Google Scholar : PubMed/NCBI

45 

Kim HM, Jeong CS, Choi HS, Kawada T and Yu R: LIGHT/TNFSF14 enhances adipose tissue inflammatory responses through its interaction with HVEM. FEBS Lett. 585:579–584. 2011. View Article : Google Scholar : PubMed/NCBI

46 

Zhou Z, Chen Y, Zhang H, Min S, Yu B, He B and Jin A: Comparison of mesenchymal stromal cells from human bone marrow and adipose tissue for the treatment of spinal cord injury. Cytotherapy. 15:434–448. 2013. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
APA
Li, J., Cao, T., Han, J., Qu, H., Jiang, S., Xie, B. ... Jiang, S. (2019). Comparison of adipose‑ and bone marrow‑derived stem cells in protecting against ox‑LDL‑induced inflammation in M1‑macrophage‑derived foam cells. Molecular Medicine Reports, 19, 2660-2670. https://doi.org/10.3892/mmr.2019.9922
MLA
Li, J., Cao, T., Han, J., Qu, H., Jiang, S., Xie, B., Yan, X., Wu, H., Liu, X., Zhang, F., Leng, X., Kang, K., Jiang, S."Comparison of adipose‑ and bone marrow‑derived stem cells in protecting against ox‑LDL‑induced inflammation in M1‑macrophage‑derived foam cells". Molecular Medicine Reports 19.4 (2019): 2660-2670.
Chicago
Li, J., Cao, T., Han, J., Qu, H., Jiang, S., Xie, B., Yan, X., Wu, H., Liu, X., Zhang, F., Leng, X., Kang, K., Jiang, S."Comparison of adipose‑ and bone marrow‑derived stem cells in protecting against ox‑LDL‑induced inflammation in M1‑macrophage‑derived foam cells". Molecular Medicine Reports 19, no. 4 (2019): 2660-2670. https://doi.org/10.3892/mmr.2019.9922