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Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways

  • Authors:
    • Jinjin Cui
    • Fengyun Zhang
    • Yongshun Wang
    • Jingjin Liu
    • Xing Ming
    • Jingbo Hou
    • Bo Lv
    • Shaohong Fang
    • Bo Yu
  • View Affiliations / Copyright

    Affiliations: Department of Cardiology, The Second Affiliated Hospital of Harbin Medical University, Harbin, Heilongjiang 150081, P.R. China, The Key Laboratory of Myocardial Ischemia, Chinese Ministry of Education, Harbin, Heilongjiang 150081, P.R. China
    Copyright: © Cui et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Pages: 1299-1309
    |
    Published online on: March 29, 2016
       https://doi.org/10.3892/ijmm.2016.2542
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Abstract

Macrophage migration inhibitory factor (MIF) has pleiotropic immune functions in a number of inflammatory diseases. Recent evidence from expression and functional studies has indicated that MIF is involved in various aspects of cardiovascular disease. In this study, we aimed to determine whether MIF supports in vitro c-kit+CD45- cardiac stem cell (CSC) survival, proliferation and differentiation into endothelial cells, as well as the possible mechanisms involved. We observed MIF receptor (CD74) expression in mouse CSCs (mCSCs) using PCR and immunofluorescence staining, and MIF secretion by mCSCs using PCR and ELISA in vitro. Increasing amounts of exogenous MIF did not affect CD74 expression, but promoted mCSC survival, proliferation and endothelial differentiation. By contrast, treatment with an MIF inhibitor (ISO-1) or siRNA targeting CD74 (CD74‑siRNA) suppressed the biological changes induced by MIF in the mCSCs. Increasing amounts of MIF increased the phosphorylation of Akt and mammalian target of rapamycin (mTOR), which are known to support cell survival, proliferation and differentiation. These effects of MIF on the mCSCs were abolished by LY294002 [a phosphoinositide 3-kinase (PI3K) inhibitor] and MK-2206 (an Akt inhibitor). Moreover, adenosine monophosphate-activated protein kinase (AMPK) phosphorylation increased following treatment with MIF. The AMPK inhibitor, compound C, partly blocked the pro-proliferative effects of MIF on the mCSCs. In conclusion, our results suggest that MIF promotes mCSC survival, proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK signaling pathways. Thus, MIF may prove to be a potential therapeutic factor in the treatment of heart failure and myocardial infarction by activating CSCs.
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View References

1 

Tang XL, Rokosh G, Sanganalmath SK, Yuan F, Sato H, Mu J, Dai S, Li C, Chen N, Peng Y, et al: Intracoronary administration of cardiac progenitor cells alleviates left ventricular dysfunction in rats with a 30-day-old infarction. Circulation. 121:293–305. 2010. View Article : Google Scholar : PubMed/NCBI

2 

Chimenti I, Smith RR, Li TS, Gerstenblith G, Messina E, Giacomello A and Marbán E: Relative roles of direct regeneration versus paracrine effects of human cardiosphere-derived cells transplanted into infarcted mice. Circ Res. 106:971–980. 2010. View Article : Google Scholar : PubMed/NCBI

3 

Rufaihah AJ, Haider HK, Heng BC, Ye L, Tan RS, Toh WS, Tian XF, Sim EK and Cao T: Therapeutic angiogenesis by transplantation of human embryonic stem cell-derived CD133+ endothelial progenitor cells for cardiac repair. Regen Med. 5:231–244. 2010. View Article : Google Scholar : PubMed/NCBI

4 

Leri A, Kajstura J and Anversa P: Role of cardiac stem cells in cardiac pathophysiology: A paradigm shift in human myocardial biology. Circ Res. 109:941–961. 2011. View Article : Google Scholar : PubMed/NCBI

5 

Williams AR and Hare JM: Mesenchymal stem cells: Biology, pathophysiology, translational findings, and therapeutic implications for cardiac disease. Circ Res. 109:923–940. 2011. View Article : Google Scholar : PubMed/NCBI

6 

Oskouei BN, Lamirault G, Joseph C, Treuer AV, Landa S, Da Silva J, Hatzistergos K, Dauer M, Balkan W, McNiece I and Hare JM: Increased potency of cardiac stem cells compared with bone marrow mesenchymal stem cells in cardiac repair. Stem Cells Transl Med. 1:116–124. 2012. View Article : Google Scholar : PubMed/NCBI

7 

Ellison GM, Vicinanza C, Smith AJ, Aquila I, Leone A, Waring CD, Henning BJ, Stirparo GG, Papait R, Scarfò M, et al: Adult c-kit(pos) cardiac stem cells are necessary and sufficient for functional cardiac regeneration and repair. Cell. 154:827–842. 2013. View Article : Google Scholar : PubMed/NCBI

8 

Chimenti C, Kajstura J, Torella D, Urbanek K, Heleniak H, Colussi C, Di Meglio F, Nadal-Ginard B, Frustaci A, Leri A, et al: Senescence and death of primitive cells and myocytes lead to premature cardiac aging and heart failure. Circ Res. 93:604–613. 2003. View Article : Google Scholar : PubMed/NCBI

9 

Dimmeler S and Leri A: Aging and disease as modifiers of efficacy of cell therapy. Circ Res. 102:1319–1330. 2008. View Article : Google Scholar : PubMed/NCBI

10 

Urbanek K, Quaini F, Tasca G, Torella D, Castaldo C, Nadal-Ginard B, Leri A, Kajstura J, Quaini E and Anversa P: Intense myocyte formation from cardiac stem cells in human cardiac hypertrophy. Proc Natl Acad Sci USA. 100:10440–10445. 2003. View Article : Google Scholar : PubMed/NCBI

11 

Urbanek K, Torella D, Sheikh F, De Angelis A, Nurzynska D, Silvestri F, Beltrami CA, Bussani R, Beltrami AP, Quaini F, et al: Myocardial regeneration by activation of multipotent cardiac stem cells in ischemic heart failure. Proc Natl Acad Sci USA. 102:8692–8697. 2005. View Article : Google Scholar : PubMed/NCBI

12 

Burger-Kentischer A, Goebel H, Seiler R, Fraedrich G, Schaefer HE, Dimmeler S, Kleemann R, Bernhagen J and Ihling C: Expression of macrophage migration inhibitory factor in different stages of human atherosclerosis. Circulation. 105:1561–1566. 2002. View Article : Google Scholar : PubMed/NCBI

13 

Calandra T, Echtenacher B, Roy DL, Pugin J, Metz CN, Hültner L, Heumann D, Männel D, Bucala R and Glauser MP: Protection from septic shock by neutralization of macrophage migration inhibitory factor. Nat Med. 6:164–170. 2000. View Article : Google Scholar : PubMed/NCBI

14 

Morand EF, Bucala R and Leech M: Macrophage migration inhibitory factor: An emerging therapeutic target in rheumatoid arthritis. Arthritis Rheum. 48:291–299. 2003. View Article : Google Scholar : PubMed/NCBI

15 

Calandra T and Roger T: Macrophage migration inhibitory factor: A regulator of innate immunity. Nat Rev Immunol. 3:791–800. 2003. View Article : Google Scholar : PubMed/NCBI

16 

Morand EF, Leech M and Bernhagen J: MIF: A new cytokine link between rheumatoid arthritis and atherosclerosis. Nat Rev Drug Discov. 5:399–410. 2006. View Article : Google Scholar : PubMed/NCBI

17 

Yu CM, Lai KW, Chen YX, Huang XR and Lan HY: Expression of macrophage migration inhibitory factor in acute ischemic myocardial injury. J Histochem Cytochem. 51:625–631. 2003. View Article : Google Scholar : PubMed/NCBI

18 

Miller EJ, Li J, Leng L, McDonald C, Atsumi T, Bucala R and Young LH: Macrophage migration inhibitory factor stimulates AMP-activated protein kinase in the ischaemic heart. Nature. 451:578–582. 2008. View Article : Google Scholar : PubMed/NCBI

19 

Qi D, Hu X, Wu X, Merk M, Leng L, Bucala R and Young LH: Cardiac macrophage migration inhibitory factor inhibits JNK pathway activation and injury during ischemia/reperfusion. J Clin Invest. 119:3807–3816. 2009. View Article : Google Scholar : PubMed/NCBI

20 

Stumptner-Cuvelette P and Benaroch P: Multiple roles of the invariant chain in MHC class II function. Biochim Biophys Acta. 1542:1–13. 2002. View Article : Google Scholar : PubMed/NCBI

21 

Leng L, Metz CN, Fang Y, Xu J, Donnelly S, Baugh J, Delohery T, Chen Y, Mitchell RA and Bucala R: MIF signal transduction initiated by binding to CD74. J Exp Med. 197:1467–1476. 2003. View Article : Google Scholar : PubMed/NCBI

22 

Ohta S, Misawa A, Fukaya R, Inoue S, Kanemura Y, Okano H, Kawakami Y and Toda M: Macrophage migration inhibitory factor (MIF) promotes cell survival and proliferation of neural stem/progenitor cells. J Cell Sci. 125:3210–3220. 2012. View Article : Google Scholar : PubMed/NCBI

23 

Schrans-Stassen B, Lue H, Sonnemans D, Bernhagen J and Post M: Stimulation of vascular smooth muscle cell migration by macrophage migration inhibitory factor. Antioxid Redox Signal. 7:1211–1216. 2005. View Article : Google Scholar : PubMed/NCBI

24 

Xiong CJ, Huang B, Zhou Y, Cun YP, Liu LT, Wang J, Li CQ, Pan Y and Wang H: Macrophage migration inhibitory factor inhibits the migration of cartilage end plate-derived stem cells by reacting with CD74. PLoS One. 7:e439842012. View Article : Google Scholar : PubMed/NCBI

25 

Xia W, Zhang F, Xie C, Jiang M and Hou M: Macrophage migration inhibitory factor confers resistance to senescence through CD74-dependent AMPK-FOXO3a signaling in mesenchymal stem cells. Stem Cell Res Ther. 6(82)2015. View Article : Google Scholar : PubMed/NCBI

26 

Palumbo S, Tsai TL and Li WJ: Macrophage migration inhibitory factor regulates AKT signaling in hypoxic culture to modulate senescence of human mesenchymal stem cells. Stem Cells Dev. 23:852–865. 2014. View Article : Google Scholar

27 

Ciuffreda L, Di Sanza C, Incani UC and Milella M: The mTOR pathway: A new target in cancer therapy. Curr Cancer Drug Targets. 10:484–495. 2010. View Article : Google Scholar : PubMed/NCBI

28 

Gao N, Zhang Z, Jiang BH and Shi X: Role of PI3K/AKT/mTOR signaling in the cell cycle progression of human prostate cancer. Biochem Biophys Res Commun. 310:1124–1132. 2003. View Article : Google Scholar : PubMed/NCBI

29 

Morgensztern D and McLeod HL: PI3K/Akt/mTOR pathway as a target for cancer therapy. Anticancer Drugs. 16:797–803. 2005. View Article : Google Scholar : PubMed/NCBI

30 

Smith AJ, Lewis FC, Aquila I, Waring CD, Nocera A, Agosti V, Nadal-Ginard B, Torella D and Ellison GM: Isolation and characterization of resident endogenous c-Kit+ cardiac stem cells from the adult mouse and rat heart. Nat Protoc. 9:1662–1681. 2014. View Article : Google Scholar : PubMed/NCBI

31 

Liu J, Wang Y, Du W, Liu W, Liu F, Zhang L, Zhang M, Hou M, Liu K, Zhang S and Yu B: Wnt1 inhibits hydrogen peroxide-induced apoptosis in mouse cardiac stem cells. PLoS One. 8:e588832013. View Article : Google Scholar : PubMed/NCBI

32 

Hou M, Cui J, Liu J, Liu F, Jiang R, Liu K, Wang Y, Yin L, Liu W and Yu B: Angiopoietin-like 4 confers resistance to hypoxia/serum deprivation-induced apoptosis through PI3K/Akt and ERK1/2 signaling pathways in mesenchymal stem cells. PLoS One. 9:e858082014. View Article : Google Scholar : PubMed/NCBI

33 

Chen J, Baydoun AR, Xu R, Deng L, Liu X, Zhu W, Shi L, Cong X, Hu S and Chen X: Lysophosphatidic acid protects mesenchymal stem cells against hypoxia and serum deprivation-induced apoptosis. Stem Cells. 26:135–145. 2008. View Article : Google Scholar

34 

White DA, Su Y, Kanellakis P, Kiriazis H, Morand EF, Bucala R, Dart AM, Gao XM and Du XJ: Differential roles of cardiac and leukocyte derived macrophage migration inhibitory factor in inflammatory responses and cardiac remodelling post myocardial infarction. J Mol Cell Cardiol. 69:32–42. 2014. View Article : Google Scholar : PubMed/NCBI

35 

Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami CA and Anversa P: Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med. 344:1750–1757. 2001. View Article : Google Scholar : PubMed/NCBI

36 

Usui T, Yamagami S, Kishimoto S, Seiich Y, Nakayama T and Amano S: Role of macrophage migration inhibitory factor in corneal neovascularization. Invest Ophthalmol Vis Sci. 48:3545–3550. 2007. View Article : Google Scholar : PubMed/NCBI

37 

Wang X, Chen T, Leng L, Fan J, Cao K, Duan Z, Zhang X, Shao C, Wu M, Tadmori I, et al: MIF produced by bone marrow-derived macrophages contributes to teratoma progression after embryonic stem cell transplantation. Cancer Res. 72:2867–2878. 2012. View Article : Google Scholar : PubMed/NCBI

38 

Chu L, Hao H, Luo M, Huang Y, Chen Z, Lu T, Zhao X, Verfaillie CM, Zweier JL and Liu Z: Ox-LDL modifies the behaviour of bone marrow stem cells and impairs their endothelial differentiation via inhibition of Akt phosphorylation. J Cell Mol Med. 15:423–432. 2011. View Article : Google Scholar

39 

Zhou Y, Pan P, Yao L, Su M, He P, Niu N, McNutt MA and Gu J: CD117-positive cells of the heart: progenitor cells or mast cells? J Histochem Cytochem. 58:309–316. 2010. View Article : Google Scholar :

40 

Moran AE, Forouzanfar MH, Roth GA, Mensah GA, Ezzati M, Flaxman A, Murray CJ and Naghavi M: The global burden of ischemic heart disease in 1990 and 2010: the Global Burden of Disease 2010 study. Circulation. 129:1493–1501. 2014. View Article : Google Scholar : PubMed/NCBI

41 

Koga K, Kenessey A, Powell SR, Sison CP, Miller EJ and Ojamaa K: Macrophage migration inhibitory factor provides cardioprotection during ischemia/reperfusion by reducing oxidative stress. Antioxid Redox Signal. 14:1191–1202. 2011. View Article : Google Scholar

42 

Ma H, Wang J, Thomas DP, Tong C, Leng L, Wang W, Merk M, Zierow S, Bernhagen J, Ren J, et al: Impaired macrophage migration inhibitory factor-AMP-activated protein kinase activation and ischemic recovery in the senescent heart. Circulation. 122:282–292. 2010. View Article : Google Scholar : PubMed/NCBI

43 

Losordo DW and Dimmeler S: Therapeutic angiogenesis and vasculogenesis for ischemic disease: part II: cell-based therapies. Circulation. 109:2692–2697. 2004. View Article : Google Scholar : PubMed/NCBI

44 

Tongers J, Losordo DW and Landmesser U: Stem and progenitor cell-based therapy in ischaemic heart disease: Promise, uncertainties, and challenges. Eur Heart J. 32:1197–1206. 2011. View Article : Google Scholar : PubMed/NCBI

45 

Hilfiker-Kleiner D, Hilfiker A, Fuchs M, Kaminski K, Schaefer A, Schieffer B, Hillmer A, Schmiedl A, Ding Z, Podewski E, et al: Signal transducer and activator of transcription 3 is required for myocardial capillary growth, control of interstitial matrix deposition, and heart protection from ischemic injury. Circ Res. 95:187–195. 2004. View Article : Google Scholar : PubMed/NCBI

46 

Salh B, Wagey R, Marotta A, Tao JS and Pelech S: Activation of phosphatidylinositol 3-kinase, protein kinase B, and p70 S6 kinases in lipopolysaccharide-stimulated Raw 264.7 cells: Differential effects of rapamycin, Ly294002, and wortmannin on nitric oxide production. J Immunol. 161:6947–6954. 1998.PubMed/NCBI

47 

Karar J and Maity A: PI3K/AKT/mTOR pathway in angiogenesis. Front Mol Neurosci. 4(51)2011. View Article : Google Scholar : PubMed/NCBI

48 

Byrne AM, Bouchier-Hayes DJ and Harmey JH: Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J Cell Mol Med. 9:777–794. 2005. View Article : Google Scholar : PubMed/NCBI

49 

Choudhary S, Hegde P, Pruitt JR, Sielecki TM, Choudhary D, Scarpato K, Degraff DJ, Pilbeam CC and Taylor JA III: Macrophage migratory inhibitory factor promotes bladder cancer progression via increasing proliferation and angiogenesis. Carcinogenesis. 34:2891–2899. 2013. View Article : Google Scholar : PubMed/NCBI

50 

Amin MA, Volpert OV, Woods JM, Kumar P, Harlow LA and Koch AE: Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ Res. 93:321–329. 2003. View Article : Google Scholar : PubMed/NCBI

51 

Russell RR III, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ and Young LH: AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J Clin Invest. 114:495–503. 2004. View Article : Google Scholar : PubMed/NCBI

52 

Dayawansa NH, Gao XM, White DA, Dart AM and Du XJ: Role of MIF in myocardial ischaemia and infarction: insight from recent clinical and experimental findings. Clin Sci (Lond). 127:149–161. 2014. View Article : Google Scholar

53 

Gao XM, Liu Y, White D, Su Y, Drew BG, Bruce CR, Kiriazis H, Xu Q, Jennings N, Bobik A, et al: Deletion of macrophage migration inhibitory factor protects the heart from severe ischemia-reperfusion injury: A predominant role of anti-inflammation. J Mol Cell Cardiol. 50:991–999. 2011. View Article : Google Scholar : PubMed/NCBI

54 

Luedike P, Hendgen-Cotta UB, Sobierajski J, Totzeck M, Reeh M, Dewor M, Lue H, Krisp C, Wolters D, Kelm M, et al: Cardioprotection through S-nitros(yl)ation of macrophage migration inhibitory factor. Circulation. 125:1880–1889. 2012. View Article : Google Scholar : PubMed/NCBI

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Copy and paste a formatted citation
Spandidos Publications style
Cui J, Zhang F, Wang Y, Liu J, Ming X, Hou J, Lv B, Fang S and Yu B: Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways. Int J Mol Med 37: 1299-1309, 2016.
APA
Cui, J., Zhang, F., Wang, Y., Liu, J., Ming, X., Hou, J. ... Yu, B. (2016). Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways. International Journal of Molecular Medicine, 37, 1299-1309. https://doi.org/10.3892/ijmm.2016.2542
MLA
Cui, J., Zhang, F., Wang, Y., Liu, J., Ming, X., Hou, J., Lv, B., Fang, S., Yu, B."Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways". International Journal of Molecular Medicine 37.5 (2016): 1299-1309.
Chicago
Cui, J., Zhang, F., Wang, Y., Liu, J., Ming, X., Hou, J., Lv, B., Fang, S., Yu, B."Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways". International Journal of Molecular Medicine 37, no. 5 (2016): 1299-1309. https://doi.org/10.3892/ijmm.2016.2542
Copy and paste a formatted citation
x
Spandidos Publications style
Cui J, Zhang F, Wang Y, Liu J, Ming X, Hou J, Lv B, Fang S and Yu B: Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways. Int J Mol Med 37: 1299-1309, 2016.
APA
Cui, J., Zhang, F., Wang, Y., Liu, J., Ming, X., Hou, J. ... Yu, B. (2016). Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways. International Journal of Molecular Medicine, 37, 1299-1309. https://doi.org/10.3892/ijmm.2016.2542
MLA
Cui, J., Zhang, F., Wang, Y., Liu, J., Ming, X., Hou, J., Lv, B., Fang, S., Yu, B."Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways". International Journal of Molecular Medicine 37.5 (2016): 1299-1309.
Chicago
Cui, J., Zhang, F., Wang, Y., Liu, J., Ming, X., Hou, J., Lv, B., Fang, S., Yu, B."Macrophage migration inhibitory factor promotes cardiac stem cell proliferation and endothelial differentiation through the activation of the PI3K/Akt/mTOR and AMPK pathways". International Journal of Molecular Medicine 37, no. 5 (2016): 1299-1309. https://doi.org/10.3892/ijmm.2016.2542
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