Surfactant protein A is expressed in the central nervous system of rats with experimental autoimmune encephalomyelitis, and suppresses inflammation in human astrocytes and microglia

Yang,Xue; Yan,Jun; Feng,Juan

doi:10.3892/mmr.2017.6441

Surfactant protein A is expressed in the central nervous system of rats with experimental autoimmune encephalomyelitis, and suppresses inflammation in human astrocytes and microglia

Authors:
- Xue Yang
- Jun Yan
- Juan Feng
View Affiliations

Affiliations: Department of Neurology, Shengjing Hospital, Affiliated Hospital of China Medical University. Shenyang, Liaoning 110004, P.R. China
Published online on: April 7, 2017 https://doi.org/10.3892/mmr.2017.6441
Pages: 3555-3565
Copyright: © Yang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The collectin surfactant protein‑A (SP‑A), a potent host defense molecule, is well recognized for its role in the maintenance of pulmonary homeostasis and the modulation of inflammatory responses. While previous studies have detected SP‑A in numerous extrapulmonary tissues, there is still a lack of information regarding its expression in central nervous system (CNS) and potential effects in neuroinflammatory diseases, such as multiple sclerosis (MS). The present study used experimental autoimmune encephalomyelitis (EAE), the most commonly used animal model of MS, to investigate the expression of SP‑A in the CNS at different stages of disease progression. In addition, in vitro experiments with lipopolysaccharide (LPS)‑stimulated human astrocytes and microglia were performed to investigate the potential role of SP‑A in the modulation of CNS inflammatory responses. The results of the present study demonstrated widespread distribution of SP‑A in the rat CNS, and also identified specific expression patterns of SP‑A at different stages of EAE. In vitro, the current study revealed that treatment of human astrocytes and microglia with LPS promoted SP‑A expression in a dose‑dependent manner. Furthermore, exogenous SP‑A protein significantly decreased Toll‑like receptor 4 and nuclear factor‑κB expression, and reduced interleukin‑1β and tumor necrosis factor‑α levels. The results of the current study indicate a potential role for SP‑A in the modulation of CNS inflammatory responses.

View Figures

View References

1	Wright JR: Immunoregulatory functions of surfactant proteins. Nat Rev Immunol. 5:58–68. 2005. View Article : Google Scholar : PubMed/NCBI
2	Chroneos ZC, Midde K, Sever-Chroneos Z and Jagannath C: Pulmonary surfactant and tuberculosis. Tuberculosis (Edinb). 89 Suppl 1:S10–S14. 2009. View Article : Google Scholar : PubMed/NCBI
3	Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, Kamran MF, Bernal AL, Reid KB, Madan T and Chakraborty T: Surfactant proteins SP-A and SP-D: Structure, function and receptors. Mol Immunol. 43:1293–1315. 2006. View Article : Google Scholar : PubMed/NCBI
4	Schaub B, Westlake RM, He H, Arestides R, Haley KJ, Campo M, Velasco G, Bellou A, Hawgood S, Poulain FR, et al: Surfactant protein D deficiency influences allergic immune responses. Clin Exp Allergy. 34:1819–1826. 2004. View Article : Google Scholar : PubMed/NCBI
5	Hartshorn KL, Crouch E, White MR, Colamussi ML, Kakkanatt A, Tauber B, Shepherd V and Sastry KN: Pulmonary surfactant proteins A and D enhance neutrophil uptake of bacteria. Am J Physiol. 274:L958–L969. 1998.PubMed/NCBI
6	Chuang CY, Chen TL and Chen RM: Molecular mechanisms of lipopolysaccharide-caused induction of surfactant protein-A gene expression in human alveolar epithelial A549 cells. Toxicol Lett. 191:132–139. 2009. View Article : Google Scholar : PubMed/NCBI
7	Yuan HT, Gowan S, Kelly FJ and Bingle CD: Cloning of guinea pig surfactant protein A defines a distinct cellular distribution pattern within the lung. Am J Physiol. 273:L900–L906. 1997.PubMed/NCBI
8	Rubio S, Lacaze-Masmonteil T, Chailley-Heu B, Kahn A, Bourbon JR and Ducroc R: Pulmonary surfactant protein A (SP-A) is expressed by epithelial cells of small and large intestine. J Biol Chem. 270:12162–12169. 1995. View Article : Google Scholar : PubMed/NCBI
9	Snyder GD, Oberley-Deegan RE, Goss KL, Romig-Martin SA, Stoll LL, Snyder JM and Weintraub NL: Surfactant protein D is expressed and modulates inflammatory responses in human coronary artery smooth muscle cells. Am J Physiol Heart Circ Physiol. 294:H2053–H2059. 2008. View Article : Google Scholar : PubMed/NCBI
10	Schob S, Schicht M, Sel S, Stiller D, Kekulé AS, Paulsen F, Maronde E and Bräuer L: The detection of surfactant proteins a, b, c and d in the human brain and their regulation in cerebral infarction, autoimmune conditions and infections of the CNS. PLoS One. 8:e744122013. View Article : Google Scholar : PubMed/NCBI
11	Quintanilla HD, Liu Y, Fatheree NY, Atkins CL, Hashmi SS, Floros J, McCormack FX, Rhoads JM and Alcorn JL: Oral administration of surfactant protein-a reduces pathology in an experimental model of necrotizing enterocolitis. J Pediatr Gastroenterol Nutr. 60:613–620. 2015. View Article : Google Scholar : PubMed/NCBI
12	Lee HM, Kang HJ, Woo JS, Chae SW, Lee SH and Hwang SJ: Upregulation of surfactant protein a in chronic rhinosinusitis. Laryngoscope. 116:328–330. 2006. View Article : Google Scholar : PubMed/NCBI
13	Wootten CT, Labadie RF, Chen A and Lane KF: Differential expression of surfactant protein A in the nasal mucosa of patients with allergy symptoms. Arch Otolaryngol Head Neck Surg. 132:1001–1007. 2006. View Article : Google Scholar : PubMed/NCBI
14	Luo JM, Wan YS, Liu ZQ, Wang GR, Floros J and Zhou HH: Regularity of distribution of immunoreactive pulmonary surfactant protein A in rat tissues. Int J Mol Med. 14:343–351. 2004.PubMed/NCBI
15	Henning LN, Azad AK, Parsa KV, Crowther JE, Tridandapani S and Schlesinger LS: Pulmonary surfactant protein a regulates TLR expression and activity in human macrophages. J Immunol. 180:7847–7858. 2008. View Article : Google Scholar : PubMed/NCBI
16	Duperray A, Barbe D, Raguenez G, Weksler BB, Romero IA, Couraud PO, Perron H and Marche PN: Inflammatory response of endothelial cells to an endogenous retrovirus associated to MS is mediated by TLR4. Int Immunol. 27:545–553. 2015. View Article : Google Scholar : PubMed/NCBI
17	Parajuli B, Sonobe Y, Kawanokuchi J, Doi Y, Noda M, Takeuchi H, Mizuno T and Suzumura A: GM-CSF increases LPS-induced production of proinflammatory mediators via upregulation of TLR4 and CD14 in murine microglia. J Neuroinflammation. 9:2682012. View Article : Google Scholar : PubMed/NCBI
18	Wu Y, Li W and Zhou C, Lu F, Gao T, Liu Y, Cao J, Zhang Y, Zhang Y and Zhou C: Ketamine inhibits lipopolysaccharide-induced astrocytes activation by suppressing TLR4/NF-ĸB pathway. Cell Physiol Biochem. 30:609–617. 2012. View Article : Google Scholar : PubMed/NCBI
19	Yao L, Kan EM, Lu J, Hao A, Dheen ST, Kaur C and Ling EA: Toll-like receptor 4 mediates microglial activation and production of inflammatory mediators in neonatal rat brain following hypoxia: Role of TLR4 in hypoxic microglia. J Neuroinflammation. 10:232013. View Article : Google Scholar : PubMed/NCBI
20	Blanco AM, Vallés SL, Pascual M and Guerri C: Involvement of TLR4/type IIL-1 receptor signaling in the induction of inflammatory mediators and cell death induced by ethanol in cultured astrocytes. J Immunol. 175:6893–6899. 2005. View Article : Google Scholar : PubMed/NCBI
21	Mohajeri M, Sadeghizadeh M and Javan M: Pertussis toxin promotes relapsing-remitting experimental autoimmune encephalomyelitis in Lewis rats. J Neuroinflammation. 289:105–110. 2015.
22	Nayak A, Dodagatta-Marri E, Tsolaki AG and Kishore U: An insight into the diverse roles of surfactant proteins, SP-A and SP-D in innate and adaptive immunity. Frontiers in immunology. 3:1312012. View Article : Google Scholar : PubMed/NCBI
23	Liu J, Hu F, Wang G, Zhou Q and Ding G: Lipopolysaccharide- induced expression of surfactant proteins A1 and A2 in human renal tubular epithelial cells. J Inflamm (Lond). 10:22013. View Article : Google Scholar : PubMed/NCBI
24	Furlan R, Cuomo C and Martino G: Animal models of multiple sclerosis. Methods Mol Biol. 549:157–173. 2009. View Article : Google Scholar : PubMed/NCBI
25	Files DK, Jausurawong T, Katrajian R and Danoff R: Multiple Sclerosis. Primary Care. 42:159–175. 2015. View Article : Google Scholar : PubMed/NCBI
26	Matsumoto Y, Ohmori K and Fujiwara M: Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system. J Neuroimmunol. 37:23–33. 1992. View Article : Google Scholar : PubMed/NCBI
27	Napoli I and Neumann H: Protective effects of microglia in multiple sclerosis. Exp Neurol. 225:24–28. 2010. View Article : Google Scholar : PubMed/NCBI
28	Lundgaard I, Osório MJ, Kress BT, Sanggaard S and Nedergaard M: White matter astrocytes in health and disease. Neuroscience. 276:161–173. 2014. View Article : Google Scholar : PubMed/NCBI
29	Awasthi S, Madhusoodhanan R and Wolf R: Surfactant protein-A and toll-like receptor-4 modulate immune functions of preterm baboon lung dendritic cell precursor cells. Cell Immunol. 268:87–96. 2011. View Article : Google Scholar : PubMed/NCBI
30	Bhatti F, Ball G, Hobbs R, Linens A, Munzar S, Akram R, Barber AJ, Anderson M, Elliott M and Edwards M: Pulmonary surfactant protein a is expressed in mouse retina by muller cells and impacts neovascularization in oxygen-induced retinopathy. Invest Ophthalmol Vis Sci. 56:232–242. 2015. View Article : Google Scholar :
31	Agrawal V, Smart K, Jilling T and Hirsch E: Surfactant Protein (SP)-A suppresses preterm delivery and inflammation via TLR2. PLoS One. 8:e6399902013. View Article : Google Scholar
32	Kawai T and Akira S: Pathogen recognition with Toll-like receptors. Curr Opin Immunol. 17:338–344. 2005. View Article : Google Scholar : PubMed/NCBI
33	Holmskov U, Lawson P, Teisner B, Tornoe I, Willis AC, Morgan C, Koch C and Reid KB: Isolation and characterization of a new member of the scavenger receptor superfamily, glycoprotein-340 (gp-340), as a lung surfactant protein-D binding molecule. J Biol Chem. 272:13743–13749. 1997. View Article : Google Scholar : PubMed/NCBI
34	Sano H, Sohma H, Muta T, Nomura S, Voelker DR and Kuroki Y: Pulmonary surfactant protein A modulates the cellular response to smooth and rough lipopolysaccharides by interaction with CD14. J Immunol. 163:387–395. 1999.PubMed/NCBI