International Urology and Nephrology

, Volume 50, Issue 4, pp 695–703 | Cite as

Collectins in urinary tract and kidney diseases

Nephrology - Review
First Online:
Received:
Accepted:
  • 114 Downloads

Abstract

The innate immune system serves as the frontline defense against invading pathogens and initiates an inflammatory response to microorganisms. Collectins are C-type lectins that are structurally characterized by a collagen-like sequence and a carbohydrate recognition domain. Moreover, they are widely expressed throughout the body and are involved in the innate immunity against a variety of pathogens, regulating inflammation, and protecting the lungs from pathogens. Recently, two classical collectins, surfactant protein A (SP-A) and surfactant protein D (SP-D), as well as novel collectin 11, were found present in urinary tract tissues. They are increasingly recognized as key players in activating the humoral arm of innate immunity and host defense in urinary tract and kidney diseases, although their biological features, functions, and mechanisms in this regard remain largely unclear. In this review, we aim to integrate results reported by ourselves and others to summarize and gain a better understanding of the functions of collectins (SP-A, SP-D, and collectin 11) in urinary tract and kidney diseases.

Keywords

Surfactant protein A Surfactant protein D Collectin 11 Innate immunity Host defense 
This is a preview of subscription content, log in to check access

Notes

Acknowledgements

Funding

This work was supported by grants from the National Natural Science Foundation of China (81300617) and Hubei Province Health and Family Planning Scientific Research Project (WJ2015Q038).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    Seaton BA, Crouch EC, McCormack FX, Head JF, Hartshorn KL, Mendelsohn R (2010) Review: structural determinants of pattern recognition by lung collectins. Innate Immun 16(3):143–150. doi: 10.1177/1753425910368716 CrossRefPubMedGoogle Scholar
  2. 2.
    Motomura W, Yoshizaki T, Ohtani K, Okumura T, Fukuda M, Fukuzawa J, Mori K, Jang SJ, Nomura N, Yoshida I, Suzuki Y, Kohgo Y, Wakamiya N (2008) Immunolocalization of a novel collectin CL-K1 in murine tissues. J Histochem Cytochem 56(3):243–252. doi: 10.1369/jhc.7A7312.2007 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Selman L, Hansen S (2012) Structure and function of collectin liver 1 (CL-L1) and collectin 11 (CL-11, CL-K1). Immunobiology 217(9):851–863. doi: 10.1016/j.imbio.2011.12.008 CrossRefPubMedGoogle Scholar
  4. 4.
    Foo SS, Reading PC, Jaillon S, Mantovani A, Mahalingam S (2015) Pentraxins and collectins: friend or Foe during pathogen invasion? Trends Microbiol 23(12):799–811. doi: 10.1016/j.tim.2015.09.006 CrossRefPubMedGoogle Scholar
  5. 5.
    Wright JR (2005) Immunoregulatory functions of surfactant proteins. Nat Rev Immunol 5(1):58–68. doi: 10.1038/nri1528 CrossRefPubMedGoogle Scholar
  6. 6.
    Ujma S, Horsnell WG, Katz AA, Clark HW, Schafer G (2017) Non-pulmonary immune functions of surfactant proteins A and D. JInnate Immun 9(1):3–11. doi: 10.1159/000451026 Google Scholar
  7. 7.
    Vieira F, Kung JW, Bhatti F (2017) Structure, genetics and function of the pulmonary associated surfactant proteins A and D: the extra-pulmonary role of these C type lectins. Ann Anat Anat Anz 211:184–201. doi: 10.1016/j.aanat.2017.03.002 CrossRefGoogle Scholar
  8. 8.
    Hu F, Ding G, Zhang Z, Gatto LA, Hawgood S, Poulain FR, Cooney RN, Wang G (2016) Innate immunity of surfactant proteins A and D in urinary tract infection with uropathogenic Escherichia coli. Innate Immun 22(1):9–20. doi: 10.1177/1753425915609973 CrossRefPubMedGoogle Scholar
  9. 9.
    Liu Z, Shi Q, Liu J, Abdel-Razek O, Xu Y, Cooney RN, Wang G (2015) Innate immune molecule surfactant protein D attenuates sepsis-induced acute pancreatic injury through modulating apoptosis and NF-kappaB-mediated inflammation. Sci Rep 5:17798. doi: 10.1038/srep17798 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Liu J, Hu F, Liang W, Wang G, Singhal PC, Ding G (2010) Polymorphisms in the Surfactant protein A gene are associated with the susceptibility to recurrent urinary tract infection in Chinese women. Tohoku J Exp Med 221(1):35–42. doi: 10.1620/tjem.221.35 CrossRefPubMedGoogle Scholar
  11. 11.
    Ma YJ, Skjoedt MO, Garred P (2013) Collectin-11/MASP complex formation triggers activation of the lectin complement pathway–the fifth lectin pathway initiation complex. J Innate Immun 5(3):242–250. doi: 10.1159/000345356 CrossRefPubMedGoogle Scholar
  12. 12.
    Saka R, Yanagihara I, Sasaki T, Nose S, Takeuchi M, Nakayama M, Okuyama H (2015) Immunolocalization of surfactant protein D in the liver from infants with cholestatic liver disease. J Pediatr Surg 50(2):297–300. doi: 10.1016/j.jpedsurg.2014.11.020 CrossRefPubMedGoogle Scholar
  13. 13.
    Ketko AK, Donn SM (2014) Surfactant-associated proteins: structure, function and clinical implications. Curr Pediatr Rev 10(2):162–167CrossRefPubMedGoogle Scholar
  14. 14.
    Waters P, Vaid M, Kishore U, Madan T (2009) Lung surfactant proteins A and D as pattern recognition proteins. Adv Exp Med Biol 653:74–97CrossRefPubMedGoogle Scholar
  15. 15.
    Gardai SJ, Xiao YQ, Dickinson M, Nick JA, Voelker DR, Greene KE, Henson PM (2003) By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115(1):13–23CrossRefPubMedGoogle Scholar
  16. 16.
    Ogasawara Y, McCormack FX, Mason RJ, Voelker DR (1994) Chimeras of surfactant proteins A and D identify the carbohydrate recognition domains as essential for phospholipid interaction. J Biol Chem 269(47):29785–29792PubMedGoogle Scholar
  17. 17.
    Guo CJ, Atochina-Vasserman EN, Abramova E, Foley JP, Zaman A, Crouch E, Beers MF, Savani RC, Gow AJ (2008) S-nitrosylation of surfactant protein-D controls inflammatory function. PLoS Biol 6(11):e266. doi: 10.1371/journal.pbio.0060266 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Haagsman HP, Hogenkamp A, van Eijk M, Veldhuizen EJ (2008) Surfactant collectins and innate immunity. Neonatology 93(4):288–294. doi: 10.1159/000121454 CrossRefPubMedGoogle Scholar
  19. 19.
    Bourbon JR, Chailley-Heu B (2001) Surfactant proteins in the digestive tract, mesentery, and other organs: evolutionary significance. Comp Biochem Physiology Part A Mol Integr Physiol 129(1):151–161CrossRefGoogle Scholar
  20. 20.
    Yadav AK, Madan T, Bernal AL (2011) Surfactant proteins A and D in pregnancy and parturition. Front Biosci (Elite Ed) 3:291–300Google Scholar
  21. 21.
    Kurimura Y, Nishitani C, Ariki S, Saito A, Hasegawa Y, Takahashi M, Hashimoto J, Takahashi S, Tsukamoto T, Kuroki Y (2012) Surfactant protein D inhibits adherence of uropathogenic Escherichia coli to the bladder epithelial cells and the bacterium-induced cytotoxicity: a possible function in urinary tract. J Biol Chem 287(47):39578–39588. doi: 10.1074/jbc.M112.380287 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Hashimoto J, Takahashi M, Saito A, Murata M, Kurimura Y, Nishitani C, Takamiya R, Uehara Y, Hasegawa Y, Hiyama Y, Sawada N, Takahashi S, Masumori N, Kuroki Y, Ariki S (2017) Surfactant protein A inhibits growth and adherence of uropathogenic Escherichia coli to protect the bladder from infection. J Immunol 198(7):2898–2905. doi: 10.4049/jimmunol.1502626 CrossRefPubMedGoogle Scholar
  23. 23.
    Hansen S, Selman L, Palaniyar N, Ziegler K, Brandt J, Kliem A, Jonasson M, Skjoedt MO, Nielsen O, Hartshorn K, Jorgensen TJ, Skjodt K, Holmskov U (2010) Collectin 11 (CL-11, CL-K1) is a MASP-1/3-associated plasma collectin with microbial-binding activity. J Immunol 185(10):6096–6104. doi: 10.4049/jimmunol.1002185 CrossRefPubMedGoogle Scholar
  24. 24.
    Farrar CA, Tran D, Li K, Wu W, Peng Q, Schwaeble W, Zhou W, Sacks SH (2016) Collectin-11 detects stress-induced L-fucose pattern to trigger renal epithelial injury. J Clin Investig 126(5):1911–1925. doi: 10.1172/JCI83000 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Wu XR, Kong XP, Pellicer A, Kreibich G, Sun TT (2009) Uroplakins in urothelial biology, function, and disease. Kidney Int 75(11):1153–1165. doi: 10.1038/ki.2009.73 CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Wu H, Kuzmenko A, Wan S, Schaffer L, Weiss A, Fisher JH, Kim KS, McCormack FX (2003) Surfactant proteins A and D inhibit the growth of Gram-negative bacteria by increasing membrane permeability. J Clin Investig 111(10):1589–1602. doi: 10.1172/JCI16889 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Kuroki Y, Takahashi M, Nishitani C (2007) Pulmonary collectins in innate immunity of the lung. Cell Microbiol 9(8):1871–1879. doi: 10.1111/j.1462-5822.2007.00953.x CrossRefPubMedGoogle Scholar
  28. 28.
    Awasthi S (2010) Surfactant protein (SP)-A and SP-D as antimicrobial and immunotherapeutic agents. Recent Pat Anti-Infect Drug Discovery 5(2):115–123CrossRefGoogle Scholar
  29. 29.
    Foxman B (2002) Epidemiology of urinary tract infections: incidence, morbidity, and economic costs. Am J Med 113(Suppl 1A):5S–13SCrossRefPubMedGoogle Scholar
  30. 30.
    Tandogdu Z, Wagenlehner FM (2016) Global epidemiology of urinary tract infections. Curr Opin Infect Dis 29(1):73–79. doi: 10.1097/QCO.0000000000000228 CrossRefPubMedGoogle Scholar
  31. 31.
    Zhou G, Mo WJ, Sebbel P, Min G, Neubert TA, Glockshuber R, Wu XR, Sun TT, Kong XP (2001) Uroplakin Ia is the urothelial receptor for uropathogenic Escherichia coli: evidence from in vitro FimH binding. J Cell Sci 114(Pt 22):4095–4103PubMedGoogle Scholar
  32. 32.
    Schilling JD, Mulvey MA, Vincent CD, Lorenz RG, Hultgren SJ (2001) Bacterial invasion augments epithelial cytokine responses to Escherichia coli through a lipopolysaccharide-dependent mechanism. J Immunol 166(2):1148–1155CrossRefPubMedGoogle Scholar
  33. 33.
    Arthur JS, Ley SC (2013) Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol 13(9):679–692. doi: 10.1038/nri3495 CrossRefPubMedGoogle Scholar
  34. 34.
    Fischer H, Lutay N, Ragnarsdottir B, Yadav M, Jonsson K, Urbano A, Al Hadad A, Ramisch S, Storm P, Dobrindt U, Salvador E, Karpman D, Jodal U, Svanborg C (2010) Pathogen specific, IRF3-dependent signaling and innate resistance to human kidney infection. PLoS Pathog 6(9):e1001109. doi: 10.1371/journal.ppat.1001109 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Chassin C, Goujon JM, Darche S, du Merle L, Bens M, Cluzeaud F, Werts C, Ogier-Denis E, Le Bouguenec C, Buzoni-Gatel D, Vandewalle A (2006) Renal collecting duct epithelial cells react to pyelonephritis-associated Escherichia coli by activating distinct TLR4-dependent and -independent inflammatory pathways. J Immunol 177(7):4773–4784CrossRefPubMedGoogle Scholar
  36. 36.
    Vandivier RW, Ogden CA, Fadok VA, Hoffmann PR, Brown KK, Botto M, Walport MJ, Fisher JH, Henson PM, Greene KE (2002) Role of surfactant proteins A, D, and C1q in the clearance of apoptotic cells in vivo and in vitro: calreticulin and CD91 as a common collectin receptor complex. J Immunol 169(7):3978–3986CrossRefPubMedGoogle Scholar
  37. 37.
    Kurihara H, Harita Y, Ichimura K, Hattori S, Sakai T (2010) SIRP-alpha-CD47 system functions as an intercellular signal in the renal glomerulus. Am J Physiol Renal Physiol 299(3):F517–527. doi: 10.1152/ajprenal.00571.2009 CrossRefPubMedGoogle Scholar
  38. 38.
    Prakoura N, Politis PK, Ihara Y, Michalak M, Charonis AS (2013) Epithelial calreticulin up-regulation promotes profibrotic responses and tubulointerstitial fibrosis development. Am J Pathol 183(5):1474–1487. doi: 10.1016/j.ajpath.2013.07.014 CrossRefPubMedGoogle Scholar
  39. 39.
    Yoshida M, Korfhagen TR, Whitsett JA (2001) Surfactant protein D regulates NF-kappa B and matrix metalloproteinase production in alveolar macrophages via oxidant-sensitive pathways. J Immunol 166(12):7514–7519CrossRefPubMedGoogle Scholar
  40. 40.
    DiAngelo S, Lin Z, Wang G, Phillips S, Ramet M, Luo J, Floros J (1999) Novel, non-radioactive, simple and multiplex PCR-cRFLP methods for genotyping human SP-A and SP-D marker alleles. Dis Markers 15(4):269–281CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Liu J, Hu F, Wang G, Zhou Q, Ding G (2013) Lipopolysaccharide-induced expression of surfactant proteins A1 and A2 in human renal tubular epithelial cells. J Inflamm 10(1):2. doi: 10.1186/1476-9255-10-2 CrossRefGoogle Scholar
  42. 42.
    Liu J, Li G, Xie WJ, Wang L, Zhang R, Huang KS, Zhou QS, Chen DC (2017) Lipopolysaccharide stimulates surfactant protein-A in human renal epithelial HK-2 Cells through upregulating toll-like receptor 4 dependent MEK1/2-ERK1/2-NF-kappaB pathway. Chin Med J 130(10):1236–1243. doi: 10.4103/0366-6999.205853 CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Silveyra P, Floros J (2013) Genetic complexity of the human surfactant-associated proteins SP-A1 and SP-A2. Gene 531(2):126–132. doi: 10.1016/j.gene.2012.09.111 CrossRefPubMedGoogle Scholar
  44. 44.
    Goto H, Mitsuhashi A, Nishioka Y (2014) Role of surfactant protein A in non-infectious lung diseases. J Med Investig JMI 61(1–2):1–6Google Scholar
  45. 45.
    Hamai K, Iwamoto H, Ishikawa N, Horimasu Y, Masuda T, Miyamoto S, Nakashima T, Ohshimo S, Fujitaka K, Hamada H, Hattori N, Kohno N (2016) Comparative study of circulating MMP-7, CCL18, KL-6, SP-A, and SP-D as disease markers of idiopathic pulmonary fibrosis. Dis Markers 2016:4759040. doi: 10.1155/2016/4759040 CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Zeisberg M, Neilson EG (2010) Mechanisms of tubulointerstitial fibrosis. J Am Soc Nephrol JASN 21(11):1819–1834. doi: 10.1681/ASN.2010080793 CrossRefPubMedGoogle Scholar
  47. 47.
    Hu F, Liang W, Ren Z, Wang G, Ding G (2012) Surfactant protein D inhibits lipopolysaccharide-induced monocyte chemoattractant protein-1 expression in human renal tubular epithelial cells: implication for tubulointerstitial fibrosis. Clin Exp Immunol 167(3):514–522. doi: 10.1111/j.1365-2249.2011.04521.x CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Tian S, Li C, Ran R, Chen SY (2017) Surfactant protein A deficiency exacerbates renal interstitial fibrosis following obstructive injury in mice. Biochem Biophys Acta 1863(2):509–517. doi: 10.1016/j.bbadis.2016.11.032 PubMedGoogle Scholar
  49. 49.
    Tian S, Zhang L, Tang J, Guo X, Dong K, Chen SY (2015) HMGB1 exacerbates renal tubulointerstitial fibrosis through facilitating M1 macrophage phenotype at the early stage of obstructive injury. Am J Physiol Renal Physiol 308(1):F69–75. doi: 10.1152/ajprenal.00484.2014 CrossRefPubMedGoogle Scholar
  50. 50.
    Taniguchi H, Kojima R, Sade H, Furuya M, Inomata N, Ito M (2007) Involvement of MCP-1 in tubulointerstitial fibrosis through massive proteinuria in anti-GBM nephritis induced in WKY rats. J Clin Immunol 27(4):409–429. doi: 10.1007/s10875-007-9085-z CrossRefPubMedGoogle Scholar
  51. 51.
    Cheung AK, Sarnak MJ, Yan G, Dwyer JT, Heyka RJ, Rocco MV, Teehan BP, Levey AS (2000) Atherosclerotic cardiovascular disease risks in chronic hemodialysis patients. Kidney Int 58(1):353–362. doi: 10.1046/j.1523-1755.2000.00173.x CrossRefPubMedGoogle Scholar
  52. 52.
    Gistera A, Hansson GK (2017) The immunology of atherosclerosis. Nat Rev Nephrol 13(6):368–380. doi: 10.1038/nrneph.2017.51 CrossRefPubMedGoogle Scholar
  53. 53.
    Bennett MR, Sinha S, Owens GK (2016) Vascular smooth muscle cells in atherosclerosis. Circ Res 118(4):692–702. doi: 10.1161/CIRCRESAHA.115.306361 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Snyder GD, Oberley-Deegan RE, Goss KL, Romig-Martin SA, Stoll LL, Snyder JM, Weintraub NL (2008) Surfactant protein D is expressed and modulates inflammatory responses in human coronary artery smooth muscle cells. Am J Physiol Heart Circ Physiol 294(5):H2053–2059. doi: 10.1152/ajpheart.91529.2007 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Sorensen GL, Madsen J, Kejling K, Tornoe I, Nielsen O, Townsend P, Poulain F, Nielsen CH, Reid KB, Hawgood S, Falk E, Holmskov U (2006) Surfactant protein D is proatherogenic in mice. Am J Physiol Heart Circ Physiol 290(6):H2286–2294. doi: 10.1152/ajpheart.01105.2005 CrossRefPubMedGoogle Scholar
  56. 56.
    Hill J, Heslop C, Man SF, Frohlich J, Connett JE, Anthonisen NR, Wise RA, Tashkin DP, Sin DD (2011) Circulating surfactant protein-D and the risk of cardiovascular morbidity and mortality. Eur Heart J 32(15):1918–1925. doi: 10.1093/eurheartj/ehr124 CrossRefPubMedGoogle Scholar
  57. 57.
    Xie F, Wang X, Ding Z, Fan P, Fan L, Chen Z, Ma G (2013) Serum surfactant protein D is associated with the prognosis in patients with chronic kidney disease. J Cardiovasc Med (Hagerstown) 14(6):461–465. doi: 10.2459/JCM.0b013e32835dbd24 CrossRefGoogle Scholar
  58. 58.
    Williams MC, Murchison JT, Edwards LD, Agusti A, Bakke P, Calverley PM, Celli B, Coxson HO, Crim C, Lomas DA, Miller BE, Rennard S, Silverman EK, Tal-Singer R, Vestbo J, Wouters E, Yates JC, van Beek EJ, Newby DE, MacNee W, Evaluation of CLtIPSEi (2014) Coronary artery calcification is increased in patients with COPD and associated with increased morbidity and mortality. Thorax 69(8):718–723. doi: 10.1136/thoraxjnl-2012-203151 CrossRefPubMedGoogle Scholar
  59. 59.
    Drueke TB, Massy ZA (2010) Atherosclerosis in CKD: differences from the general population. Nat Rev Nephrol 6(12):723–735. doi: 10.1038/nrneph.2010.143 CrossRefPubMedGoogle Scholar
  60. 60.
    Moe SM, Chen NX (2008) Mechanisms of vascular calcification in chronic kidney disease. J Am Soc Nephrol JASN 19(2):213–216. doi: 10.1681/ASN.2007080854 CrossRefPubMedGoogle Scholar
  61. 61.
    Hu F, Zhong Q, Gong J, Qin Y, Cui L, Yuan H (2016) Serum surfactant protein D is associated with atherosclerosis of the carotid artery in patients on maintenance hemodialysis. Clin Lab 62(1–2):97–104PubMedGoogle Scholar
  62. 62.
    Goncalves GM, Zamboni DS, Camara NO (2010) The role of innate immunity in septic acute kidney injuries. Shock 34(Suppl 1):22–26. doi: 10.1097/SHK.0b013e3181e7e69e CrossRefPubMedGoogle Scholar
  63. 63.
    Liu J, Abdel-Razek O, Liu Z, Hu F, Zhou Q, Cooney RN, Wang G (2015) Role of surfactant proteins A and D in sepsis-induced acute kidney injury. Shock 43(1):31–38. doi: 10.1097/SHK.0000000000000270 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Liu J, Li G, Li L, Liu Z, Zhou Q, Wang G, Chen D (2017) Surfactant protein-D (SP-D) gene polymorphisms and serum level as predictors of susceptibility and prognosis of acute kidney injury in the Chinese population. BMC Nephrol 18(1):67. doi: 10.1186/s12882-017-0485-x CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Ishii T, Hagiwara K, Ikeda S, Arai T, Mieno MN, Kumasaka T, Muramatsu M, Sawabe M, Gemma A, Kida K (2012) Association between genetic variations in surfactant protein d and emphysema, interstitial pneumonia, and lung cancer in a Japanese population. Copd 9(4):409–416. doi: 10.3109/15412555.2012.676110 CrossRefPubMedGoogle Scholar
  66. 66.
    Keshi H, Sakamoto T, Kawai T, Ohtani K, Katoh T, Jang SJ, Motomura W, Yoshizaki T, Fukuda M, Koyama S, Fukuzawa J, Fukuoh A, Yoshida I, Suzuki Y, Wakamiya N (2006) Identification and characterization of a novel human collectin CL-K1. Microbiol Immunol 50(12):1001–1013CrossRefPubMedGoogle Scholar
  67. 67.
    Yoshizaki T, Ohtani K, Motomura W, Jang SJ, Mori K, Kitamoto N, Yoshida I, Suzuki Y, Wakamiya N (2012) Comparison of human blood concentrations of collectin kidney 1 and mannan-binding lectin. J Biochem 151(1):57–64. doi: 10.1093/jb/mvr114 CrossRefPubMedGoogle Scholar
  68. 68.
    Ali YM, Lynch NJ, Haleem KS, Fujita T, Endo Y, Hansen S, Holmskov U, Takahashi K, Stahl GL, Dudler T, Girija UV, Wallis R, Kadioglu A, Stover CM, Andrew PW, Schwaeble WJ (2012) The lectin pathway of complement activation is a critical component of the innate immune response to pneumococcal infection. PLoS Pathog 8(7):e1002793. doi: 10.1371/journal.ppat.1002793 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Yongfang Qin
    • 1
  • Jingjing Liu
    • 1
  • Jiao Liu
    • 2
  • Fengqi Hu
    • 1
  1. 1.Department of NephrologyXiangyang Central Hospital, Hubei University of Arts and ScienceXiangyangChina
  2. 2.Department of Critical Care MedicineRenmin Hospital of Wuhan UniversityWuhanChina

Personalised recommendations