Top

Published in:

01-03-2018 | ORIGINAL ARTICLE

Apolipoprotein M Protects Against Lipopolysaccharide-Induced Acute Lung Injury via Sphingosine-1-Phosphate Signaling

Authors: Bin Zhu, Guang-hua Luo, Yue-hua Feng, Miao-mei Yu, Jun Zhang, Jiang Wei, Chun Yang, Ning Xu, Xiao-ying Zhang

Published in: Inflammation | Issue 2/2018

Abstract

It had been demonstrated that apolipoprotein M (apoM) is an important carrier of sphingosine-1-phosphate (S1P) in blood, and the S1P has critical roles in the pathogenesis of sepsis-induced acute lung injury (ALI). In the present study, we investigated whether apoM has beneficial effects in a mouse model after lipopolysaccharide (LPS)-induced ALI. Forty-eight mice were divided into two groups: male C57BL/6 wild-type (apoM^+/+) group (n = 24) and apoM gene-deficient (apoM^−/−) group (n = 24) and then randomly subdivided into four subgroups (n = 6 each) according to different intraperitoneal (i.p.) injection: control group, W146 group, LPS group, and LPS + W146 group. Serum levels of interleukin-1 beta (IL-1β) and mRNA levels of IL-1β, interleukin-6 (IL-6), and tumor necrosis factor-α (TNF-α), lung histology, wet/dry weight ratio, and immunohistochemistry were measured at 3 h after the baseline and compared in each group. Our results clearly demonstrated that IL-1β mRNA levels and other inflammatory biomarkers were significantly increased in the lungs of LPS-induced ALI apoM^−/− mice compared to those of the apoM^+/+ mice. Moreover, when apoM^+/+ mice were treated with W146, a S1P receptor (S1PR1) antagonist, these inflammatory biomarkers could be significantly upregulated by LPS-induced ALI. Therefore, it suggests that apoM-S1P-S1PR1 signaling might underlie the pathogenesis of ALI and apoM could have physiological benefits to alleviate LPS-induced ALI.

Dellinger, R.P., M.M. Levy, A. Rhodes, D. Annane, H. Gerlach, S.M. Opal, J.E. Sevransky, C.L. Sprung, I.S. Douglas, R. Jaeschke, T.M. Osborn, M.E. Nunnally, S.R. Townsend, K. Reinhart, R.M. Kleinpell, D.C. Angus, C.S. Deutschman, F.R. Machado, G.D. Rubenfeld, S. Webb, R.J. Beale, J.L. Vincent, and R. Moreno. 2013. Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Medicine 39 (2): 165–228.PubMedCrossRef

Chenaud, C., P.G. Merlani, P. Roux-Lombard, D. Burger, S. Harbarth, S. Luyasu, J.D. Graf, J.M. Dayer, and B. Ricou. 2004. Low apolipoprotein A-I level at intensive care unit admission and systemic inflammatory response syndrome exacerbation. Critical Care Medicine 32 (3): 632–637.PubMedCrossRef

Vermont, C.L., M. den Brinker, N. Kakeci, E.D. de Kleijn, Y.B. de Rijke, K.F. Joosten, R. de Groot, and J.A. Hazelzet. 2005. Serum lipids and disease severity in children with severe meningococcal sepsis. Critical Care Medicine 33 (7): 1610–1615.PubMedCrossRef

Chien, J.Y., J.S. Jerng, Yu CJ, and P.C. Yang. 2005. Low serum level of high-density lipoprotein cholesterol is a poor prognostic factor for severe sepsis. Critical Care Medicine 33 (8): 1688–1693.PubMedCrossRef

Berbee, J.F., C.C. van der Hoogt, C.J. de Haas, K.P. van Kessel, G.M. Dallinga-Thie, J.A. Romijn, L.M. Havekes, H.J. van Leeuwen, and P.C. Rensen. 2008. Plasma apolipoprotein CI correlates with increased survival in patients with severe sepsis. Intensive Care Medicine 34 (5): 907–911.PubMedCrossRef

Barlage, S., C. Gnewuch, G. Liebisch, Z. Wolf, F.X. Audebert, T. Gluck, D. Frohlich, B.K. Kramer, G. Rothe, and G. Schmitz. 2009. Changes in HDL-associated apolipoproteins relate to mortality in human sepsis and correlate to monocyte and platelet activation. Intensive Care Medicine 35 (11): 1877–1885.PubMedCrossRef

Grion, C.M., L.T. Cardoso, T.F. Perazolo, A.S. Garcia, D.S. Barbosa, H.K. Morimoto, T. Matsuo, and A.J. Carrilho. 2010. Lipoproteins and CETP levels as risk factors for severe sepsis in hospitalized patients. European Journal of Clinical Investigation 40 (4): 330–338.PubMedCrossRef

Cohen, J. 2002. The immunopathogenesis of sepsis. Nature 420 (6917): 885–891.PubMedCrossRef

Hotchkiss, R.S., and I.E. Karl. 2003. The pathophysiology and treatment of sepsis. The New England Journal of Medicine 348 (2): 138–150.PubMedCrossRef

10.

Annane, D., E. Bellissant, and J.M. Cavaillon. 2005. Septic shock. Lancet 365 (9453): 63–78.PubMedCrossRef

11.

Dellinger, R.P., M.M. Levy, J.M. Carlet, J. Bion, M.M. Parker, R. Jaeschke, K. Reinhart, D.C. Angus, C. Brun-Buisson, R. Beale, T. Calandra, J.F. Dhainaut, H. Gerlach, M. Harvey, J.J. Marini, J. Marshall, M. Ranieri, G. Ramsay, J. Sevransky, B.T. Thompson, S. Townsend, J.S. Vender, J.L. Zimmerman, and J.L. Vincent. 2008. Surviving sepsis campaign: international guidelines for management of severe sepsis and septic shock: 2008. Intensive Care Medicine 34 (1): 17–60.PubMedCrossRef

12.

Roy, S.K., D. Kendrick, B.D. Sadowitz, L. Gatto, K. Snyder, J.M. Satalin, L.M. Golub, and G. Nieman. 2011. Jack of all trades: pleiotropy and the application of chemically modified tetracycline-3 in sepsis and the acute respiratory distress syndrome (ARDS). Pharmacological Research 64 (6): 580–589.PubMedPubMedCentralCrossRef

13.

Parikh, S.M. 2013. Dysregulation of the angiopoietin-Tie-2 axis in sepsis and ARDS. Virulence 4 (6): 517–524.PubMedPubMedCentralCrossRef

14.

Ranieri, V.M., G.D. Rubenfeld, B.T. Thompson, N.D. Ferguson, E. Caldwell, E. Fan, L. Camporota, and A.S. Slutsky. 2012. Acute respiratory distress syndrome: the Berlin Definition. JAMA 307 (23): 2526–2533.PubMed

15.

Bernard, G.R., A. Artigas, K.L. Brigham, J. Carlet, K. Falke, L. Hudson, M. Lamy, J.R. Legall, A. Morris, and R. Spragg. 1994. The American-European Consensus Conference on ARDS. Definitions, mechanisms, relevant outcomes, and clinical trial coordination. American Journal of Respiratory and Critical Care Medicine 149 (3 Pt 1): 818–824.PubMedCrossRef

16.

Ferguson, N.D., A.M. Davis, A.S. Slutsky, and T.E. Stewart. 2005. Development of a clinical definition for acute respiratory distress syndrome using the Delphi technique. Journal of Critical Care 20 (2): 147–154.PubMedCrossRef

17.

Kangelaris, K.N., A. Prakash, K.D. Liu, B. Aouizerat, P.G. Woodruff, D.J. Erle, A. Rogers, E.J. Seeley, J. Chu, T. Liu, T. Osterberg-Deiss, H. Zhuo, M.A. Matthay, and C.S. Calfee. 2015. Increased expression of neutrophil-related genes in patients with early sepsis-induced ARDS. American Journal of Physiology. Lung Cellular and Molecular Physiology 308 (11): L1102–L1113.PubMedPubMedCentralCrossRef

18.

Petroni, R.C., P.J. Biselli, T.M. de Lima, M.C. Theobaldo, E.T. Caldini, R.N. Pimentel, H.V. Barbeiro, S.A. Kubo, I.T. Velasco, and F.G. Soriano. 2015. Hypertonic saline (NaCl 7.5%) reduces LPS-induced acute lung injury in rats. Inflammation 38 (6): 2026–2035.PubMedCrossRef

19.

Kuebler, W.M., J. Borges, A. Sckell, G.E. Kuhnle, K. Bergh, K. Messmer, and A.E. Goetz. 2000. Role of L-selectin in leukocyte sequestration in lung capillaries in a rabbit model of endotoxemia. American Journal of Respiratory and Critical Care Medicine 161 (1): 36–43.PubMedCrossRef

20.

Ware, L.B., and M.A. Matthay. 2000. The acute respiratory distress syndrome. The New England Journal of Medicine 342 (18): 1334–1349.PubMedCrossRef

21.

Densmore, J.C., P.R. Signorino, J. Ou, O.A. Hatoum, J.J. Rowe, Y. Shi, S. Kaul, D.W. Jones, R.E. Sabina, K.A. Pritchard Jr., K.S. Guice, and K.T. Oldham. 2006. Endothelium-derived microparticles induce endothelial dysfunction and acute lung injury. Shock 26 (5): 464–471.PubMedCrossRef

22.

Wang, X., K.B. Adler, J. Erjefalt, and C. Bai. 2007. Airway epithelial dysfunction in the development of acute lung injury and acute respiratory distress syndrome. Expert Review of Respiratory Medicine 1 (1): 149–155.PubMedCrossRef

23.

Hla, T., M.J. Lee, N. Ancellin, S. Thangada, C.H. Liu, M. Kluk, S.S. Chae, and M.T. Wu. 2000. Sphingosine-1-phosphate signaling via the EDG-1 family of G-protein-coupled receptors. Annals of the New York Academy of Sciences 905: 16–24.PubMedCrossRef

24.

Im, D.S., A.R. Ungar, and K.R. Lynch. 2000. Characterization of a zebrafish (Danio rerio) sphingosine 1-phosphate receptor expressed in the embryonic brain. Biochemical and Biophysical Research Communications 279 (1): 139–143.PubMedCrossRef

25.

Pyne, S., and N. Pyne. 2000. Sphingosine 1-phosphate signalling via the endothelial differentiation gene family of G-protein-coupled receptors. Pharmacology & Therapeutics 88 (2): 115–131.CrossRef

26.

Anliker, B., and J. Chun. 2004. Cell surface receptors in lysophospholipid signaling. Seminars in Cell & Developmental Biology 15 (5): 457–465.CrossRef

27.

Rosen, H., and E.J. Goetzl. 2005. Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nature Reviews. Immunology 5 (7): 560–570.PubMedCrossRef

28.

Camerer, E., J.B. Regard, I. Cornelissen, Y. Srinivasan, D.N. Duong, D. Palmer, T.H. Pham, J.S. Wong, R. Pappu, and S.R. Coughlin. 2009. Sphingosine-1-phosphate in the plasma compartment regulates basal and inflammation-induced vascular leak in mice. The Journal of Clinical Investigation 119 (7): 1871–1879.PubMedPubMedCentral

29.

Christoffersen, C., and L.B. Nielsen. 2013. Apolipoprotein M: bridging HDL and endothelial function. Current Opinion in Lipidology 24 (4): 295–300.PubMedCrossRef

30.

Sammani, S., L. Moreno-Vinasco, T. Mirzapoiazova, P.A. Singleton, E.T. Chiang, C.L. Evenoski, T. Wang, B. Mathew, A. Husain, J. Moitra, X. Sun, L. Nunez, J.R. Jacobson, S.M. Dudek, V. Natarajan, and J.G. Garcia. 2010. Differential effects of sphingosine 1-phosphate receptors on airway and vascular barrier function in the murine lung. American Journal of Respiratory Cell and Molecular Biology 43 (4): 394–402.PubMedCrossRef

31.

Xu, N., and B. Dahlback. 1999. A novel human apolipoprotein (apoM). The Journal of Biological Chemistry 274 (44): 31286–31290.PubMedCrossRef

32.

Feingold, K.R., J.K. Shigenaga, L.G. Chui, A. Moser, W. Khovidhunkit, and C. Grunfeld. 2008. Infection and inflammation decrease apolipoprotein M expression. Atherosclerosis 199 (1): 19–26.PubMedCrossRef

33.

Christoffersen, C., H. Obinata, S.B. Kumaraswamy, S. Galvani, J. Ahnstrom, M. Sevvana, C. Egerer-Sieber, Y.A. Muller, T. Hla, L.B. Nielsen, and B. Dahlback. 2011. Endothelium-protective sphingosine-1-phosphate provided by HDL-associated apolipoprotein M. Proceedings of the National Academy of Sciences of the United States of America 108 (23): 9613–9618.PubMedPubMedCentralCrossRef

34.

Rodriguez, C., M. Gonzalez-Diez, L. Badimon, and J. Martinez-Gonzalez. 2009. Sphingosine-1-phosphate: a bioactive lipid that confers high-density lipoprotein with vasculoprotection mediated by nitric oxide and prostacyclin. Thrombosis and Haemostasis 101 (4): 665–673.PubMed

35.

Wang, Z., G. Luo, Y. Feng, L. Zheng, H. Liu, Y. Liang, Z. Liu, P. Shao, M. Berggren-Soderlund, X. Zhang, and N. Xu. 2015. Decreased splenic CD4(+) T-lymphocytes in apolipoprotein M gene deficient mice. BioMed Research International 2015: 293512.PubMedPubMedCentral

36.

Szarka, R.J., N. Wang, L. Gordon, P.N. Nation, and R.H. Smith. 1997. A murine model of pulmonary damage induced by lipopolysaccharide via intranasal instillation. Journal of Immunological Methods 202 (1): 49–57.PubMedCrossRef

37.

Smith, K.M., J.D. Mrozek, S.C. Simonton, D.R. Bing, P.A. Meyers, J.E. Connett, and M.C. Mammel. 1997. Prolonged partial liquid ventilation using conventional and high-frequency ventilatory techniques: gas exchange and lung pathology in an animal model of respiratory distress syndrome. Critical Care Medicine 25 (11): 1888–1897.PubMedCrossRef

38.

Nahum, A., J. Hoyt, L. Schmitz, J. Moody, R. Shapiro, and J.J. Marini. 1997. Effect of mechanical ventilation strategy on dissemination of intratracheally instilled Escherichia coli in dogs. Critical Care Medicine 25 (10): 1733–1743.PubMedCrossRef

39.

Rotta, A.T., and D.M. Steinhorn. 1998. Partial liquid ventilation reduces pulmonary neutrophil accumulation in an experimental model of systemic endotoxemia and acute lung injury. Critical Care Medicine 26 (10): 1707–1715.PubMedCrossRef

40.

Luo, G., X. Zhang, Q. Mu, L. Chen, L. Zheng, J. Wei, M. Berggren-Soderlund, P. Nilsson-Ehle, and N. Xu. 2010. Expression and localization of apolipoprotein M in human colorectal tissues. Lipids in Health and Disease 9: 102.PubMedPubMedCentralCrossRef

41.

Hammes, L.S., R.R. Tekmal, P. Naud, M.I. Edelweiss, N. Kirma, P.T. Valente, K.J. Syrjanen, and J.S. Cunha-Filho. 2008. Up-regulation of VEGF, c-fms and COX-2 expression correlates with severity of cervical cancer precursor (CIN) lesions and invasive disease. Gynecologic Oncology 110 (3): 445–451.PubMedCrossRef

42.

Rubenfeld, G.D., E. Caldwell, E. Peabody, J. Weaver, D.P. Martin, M. Neff, E.J. Stern, and L.D. Hudson. 2005. Incidence and outcomes of acute lung injury. The New England Journal of Medicine 353 (16): 1685–1693.PubMedCrossRef

43.

Steinhauser, M.L., S.L. Kunkel, and C.M. Hogaboam. 1999. New Frontiers in cytokine involvement during experimental sepsis. ILAR Journal 40 (4): 142–150.PubMedCrossRef

44.

Khovidhunkit, W., M.S. Kim, R.A. Memon, J.K. Shigenaga, A.H. Moser, K.R. Feingold, and C. Grunfeld. 2004. Effects of infection and inflammation on lipid and lipoprotein metabolism: mechanisms and consequences to the host. Journal of Lipid Research 45 (7): 1169–1196.PubMedCrossRef

45.

Chen, H., C. Bai, and X. Wang. 2010. The value of the lipopolysaccharide-induced acute lung injury model in respiratory medicine. Expert Review of Respiratory Medicine 4 (6): 773–783.PubMedCrossRef

46.

Tong, Q., L. Zheng, Q. Kang, O.J. Dodd, J. Langer, B. Li, D. Wang, and D. Li. 2006. Upregulation of hypoxia-induced mitogenic factor in bacterial lipopolysaccharide-induced acute lung injury. FEBS Letters 580 (9): 2207–2215.PubMedCrossRef

47.

Melo, A.C., S.S. Valenca, L.B. Gitirana, J.C. Santos, M.L. Ribeiro, M.N. Machado, C.B. Magalhaes, W.A. Zin, and L.C. Porto. 2013. Redox markers and inflammation are differentially affected by atorvastatin, pravastatin or simvastatin administered before endotoxin-induced acute lung injury. International Immunopharmacology 17 (1): 57–64.PubMedCrossRef

48.

He, Z., X. Chen, S. Wang, and Z. Zou. 2014. Toll-like receptor 4 monoclonal antibody attenuates lipopolysaccharide-induced acute lung injury in mice. Experimental and Therapeutic Medicine 8 (3): 871–876.PubMedPubMedCentralCrossRef

49.

Wittwer, T., U.F. Franke, M. Ochs, T. Sandhaus, A. Schuette, S. Richter, N. Dreyer, L. Knudsen, T. Muller, H. Schubert, J. Richter, and T. Wahlers. 2005. Inhalative pre-treatment of donor lungs using the aerosolized prostacyclin analog iloprost ameliorates reperfusion injury. The Journal of heart and lung transplantation : the official publication of the International Society for Heart Transplantation 24 (10): 1673–1679.CrossRef

50.

Katzenstein, A.L., C.M. Bloor, and A.A. Leibow. 1976. Diffuse alveolar damage—the role of oxygen, shock, and related factors. A review. The American Journal of Pathology 85 (1): 209–228.PubMedPubMedCentral

51.

Thille, A.W., A. Esteban, P. Fernandez-Segoviano, J.M. Rodriguez, J.A. Aramburu, O. Penuelas, I. Cortes-Puch, P. Cardinal-Fernandez, J.A. Lorente, and F. Frutos-Vivar. 2013. Comparison of the berlin definition for acute respiratory distress syndrome with autopsy. American Journal of Respiratory and Critical Care Medicine 187 (7): 761–767.PubMedCrossRef

52.

Zhao, Y., I.A. Gorshkova, E. Berdyshev, D. He, P. Fu, W. Ma, Y. Su, P.V. Usatyuk, S. Pendyala, B. Oskouian, J.D. Saba, J.G. Garcia, and V. Natarajan. 2011. Protection of LPS-induced murine acute lung injury by sphingosine-1-phosphate lyase suppression. American Journal of Respiratory Cell and Molecular Biology 45 (2): 426–435.PubMedCrossRef

53.

Liu, J., P.S. Zhang, Q. Yu, L. Liu, Y. Yang, and H.B. Qiu. 2012. Kinetic and distinct distribution of conventional dendritic cells in the early phase of lipopolysaccharide-induced acute lung injury. Molecular Biology Reports 39 (12): 10421–10431.PubMedCrossRef

54.

Kumaraswamy, S.B., A. Linder, P. Akesson, and B. Dahlback. 2012. Decreased plasma concentrations of apolipoprotein M in sepsis and systemic inflammatory response syndromes. Critical Care 16 (2): R60.PubMedPubMedCentralCrossRef

55.

Mihara, Y., T. Miyamoto, Y. Hagari, and M. Mihara. 1997. Rudimentary meningocele of the scalp. The Journal of Dermatology 24 (9): 606–610.PubMedCrossRef

56.

Blaho, V.A., and T. Hla. 2011. Regulation of mammalian physiology, development, and disease by the sphingosine 1-phosphate and lysophosphatidic acid receptors. Chemical Reviews 111 (10): 6299–6320.PubMedPubMedCentralCrossRef

Title: Apolipoprotein M Protects Against Lipopolysaccharide-Induced Acute Lung Injury via Sphingosine-1-Phosphate Signaling
Authors: Bin Zhu
Guang-hua Luo
Yue-hua Feng
Miao-mei Yu
Jun Zhang
Jiang Wei
Chun Yang
Ning Xu
Xiao-ying Zhang
Publication date: 01-03-2018
Publisher: Springer US
Published in: Inflammation / Issue 2/2018
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI: https://doi.org/10.1007/s10753-017-0719-x

ACC 2024 Congress Coverage

Heart Failure Video

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Apolipoprotein M Protects Against Lipopolysaccharide-Induced Acute Lung Injury via Sphingosine-1-Phosphate Signaling

Abstract

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 2/2018

Umbelliferone Alleviates Myocardial Ischemia: the Role of Inflammation and Apoptosis

α7-nAChR Activation Has an Opposite Effect on Healing of Covered and Uncovered Wounds

Cardioprotective Effects of Morroniside in Rats Following Acute Myocardial Infarction

Curc-mPEG454, a PEGylated Curcumin Derivative, Improves Anti-inflammatory and Antioxidant Activities: a Comparative Study

Characteristic Comparison of Meningitis and Non-meningitis of Streptococcus suis in an Experimentally Infected Porcine Model

Changes in Neutrophil Metabolism upon Activation and Aging

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page