Sialic acid: an attractive biomarker with promising biomedical applications

Doostkam, Aida; Malekmakan, Leila; Hosseinpour, Alireza; Janfeshan, Sahar; Roozbeh, Jamshid; Masjedi, Fatemeh

doi:10.2478/abm-2022-0020

Abstract

This broad, narrative review highlights the roles of sialic acids as acidic sugars found on cellular membranes. The role of sialic acids in cellular communication and development has been well established. Recently, attention has turned to the fundamental role of sialic acids in many diseases, including viral infections, cardiovascular diseases, neurological disorders, diabetic nephropathy, and malignancies. Sialic acid may be a target for developing new drugs to treat various cancers and inflammatory processes. We recommend the routine measurement of serum sialic acid as a sensitive inflammatory marker in various diseases.

References

Park SS. Post-glycosylation modification of sialic acid and its role in virus pathogenesis. Vaccines (Basel). 2019; 7:171. doi: 10.3390/vaccines7040171
Open DOI Search in Google Scholar Back to article
Zhang C, Chen J, Liu Y, Xu D. Sialic acid metabolism as a potential therapeutic target of atherosclerosis. Lipids Health Dis. 2019; 18:173. doi: 10.1186/s12944-019-1113-5
Open DOI Search in Google Scholar Back to article
Schauer R, Kamerling JP. Exploration of the sialic acid world. In: Baker DC, editor. Sialic acids, Part I: Historical background and development, and chemical synthesis. San Diego: Academic Press; 2018, p. 1–213. (Demchenko A, Knirel YA, Stütz AE, Vliegenthart JFG, Yu B, series advisors. Adv Carbohydr Chem Biochem., vol. 75).
Search in Google Scholar Back to article
Roozbeh J, Merat A, Bodagkhan F, Afshariani R, Yarmohammadi H. Significance of serum and urine neuraminidase activity and serum and urine level of sialic acid in diabetic nephropathy. Int Urol Nephrol. 2011; 43:1143–8.
Search in Google Scholar Back to article
Zhu Z, Cai T, Fan L, Lou K, Hua X, Huang Z, Gao G. Clinical value of immune-inflammatory parameters to assess the severity of coronavirus disease 2019. Int J Infect Dis. 2020; 95:332–9.
Search in Google Scholar Back to article
Matrosovich M, Herrler G, Klenk HD. Sialic acid receptors of viruses. In: Gerardy-Schahn R, Delannoy P, von Itzstein M, editors. Sialoglyco chemistry and biology II: tools and techniques to identify and capture sialoglycans. Heidelberg: Springer-Verlag; 2015, p. 1–28. (H. Bayley H, Houk KN, Hughes G, Hunter CA, Ishihara K, M.J. Krische MJ, et al., series editors. Top Curr Chem., vol. 367).
Search in Google Scholar Back to article
Wasik BR, Barnard KN, Parrish CR. Effects of sialic acid modifications on virus binding and infection. Trends Microbiol. 2016; 24:991–1001.
Search in Google Scholar Back to article
von Itzstein M., editor. Influenza virus sialidase – A drug discovery target. Basel: Springer; 2014, p. 1–178. (Parnham MJ, Bruinvels J., series editors., Milestones Drug Ther.).
Search in Google Scholar Back to article
Wu NC, Wilson IA. Structural biology of influenza hemagglutinin: an amaranthine adventure. Viruses. 2020; 12:1053. doi: 10.3390/v12091053
Open DOI Search in Google Scholar Back to article
Benton DJ, Wharton SA, Martin SR, McCauley JW. Role of neuraminidase in influenza A(H7N9) virus receptor binding. J Virol. 2017; 91:e02293–16. doi: 10.1128/jvi.02293-16
Open DOI Search in Google Scholar Back to article
Wen F, Wan X-F. Influenza neuraminidase: underrated role in receptor binding. Trends Microbiol. 2019; 27:477–9.
Search in Google Scholar Back to article
Imai M, Kawaoka Y. The role of receptor binding specificity in interspecies transmission of influenza viruses. Curr Opin Virol. 2012; 2:160–7.
Search in Google Scholar Back to article
Matrosovich M, Tuzikov A, Bovin N, Gambaryan A, Klimov A, Castrucci MR, et al. Early alterations of the receptor-binding properties of H1, H2, and H3 avian influenza virus hemagglutinins after their introduction into mammals. J Virol. 2000; 74:8502–12.
Search in Google Scholar Back to article
Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology. 1983; 127:361–73.
Search in Google Scholar Back to article
Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology. 1994; 205:17–23.
Search in Google Scholar Back to article
Wang M, Veit M. Hemagglutinin-esterase-fusion (HEF) protein of influenza C virus. Protein Cell. 2016; 7:28–45.
Search in Google Scholar Back to article
Kim C-H. SARS-CoV-2 Evolutionary adaptation toward host entry and recognition of receptor O-acetyl sialylation in virus-host interaction. Int J Mol Sci. 2020; 21:4549. doi: 10.3390/ijms21124549
Open DOI Search in Google Scholar Back to article
Bolton MJ, Ort JT, McBride R, Swanson NJ, Wilson J, Awofolaju M, et al. Antigenic and virological properties of an H3N2 variant that continues to dominate the 2021–22 Northern Hemisphere influenza season. Cell Rep. 2022; 39:110897. doi: 10.1016/j.celrep.2022.110897
Open DOI Search in Google Scholar Back to article
Klausegger A, Strobl B, Regl G, Kaser A, Luytjes W, Vlasak R. Identification of a coronavirus hemagglutinin-esterase with a substrate specificity different from those of influenza C virus and bovine coronavirus. J Virol. 1999; 73:3737–43.
Search in Google Scholar Back to article
Smits SL, Gerwig GJ, van Vliet AL, Lissenberg A, Briza P, Kamerling JP, et al. Nidovirus sialate-O-acetylesterases: evolution and substrate specificity of coronaviral and toroviral receptor-destroying enzymes. J Biol Chem. 2005; 280:6933–41.
Search in Google Scholar Back to article
Markwell MA, Svennerholm L, Paulson JC. Specific gangliosides function as host cell receptors for Sendai virus. Proc Natl Acad Sci U S A. 1981; 78:5406–10.
Search in Google Scholar Back to article
Suzuki T, Portner A, Scroggs RA, Uchikawa M, Koyama N, Matsuo K, et al. Receptor specificities of human respiroviruses. J Virol. 2001; 75:4604–13.
Search in Google Scholar Back to article
Palese P, Tobita K, Ueda M, Compans RW. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology. 1974; 61:397–410.
Search in Google Scholar Back to article
Vlasak R, Luytjes W, Spaan W, Palese P. Human and bovine coronaviruses recognize sialic acid-containing receptors similar to those of influenza C viruses. Proc Natl Acad Sci U S A. 1988; 85:4526–9.
Search in Google Scholar Back to article
Heida R, Bhide YC, Gasbarri M, Kocabiyik Ö, Stellacci F, Huckriede ALW, et al. Advances in the development of entry inhibitors for sialic-acid-targeting viruses. Drug Discov Today. 2021; 26:122–37.
Search in Google Scholar Back to article
Qing E, Hantak M, Perlman S, Gallagher T. Distinct roles for sialoside and protein receptors in coronavirus infection. mBio. 2020; 11:e02764–19. doi: 10.1128/mBio.02764-19
Open DOI Search in Google Scholar Back to article
Munkley J, Scott E. Targeting aberrant sialylation to treat cancer. Medicines (Basel). 2019; 6:102. doi: 10.3390/medicines6040102
Open DOI Search in Google Scholar Back to article
Daly J, Carlsten M, O’Dwyer M. Sugar free: novel immunotherapeutic approaches targeting Siglecs and sialic acids to enhance natural killer cell cytotoxicity against cancer. Front Immunol. 2019; 10:1047. doi: 10.3389/fimmu.2019.01047
Open DOI Search in Google Scholar Back to article
Glavey SV, Manier S, Natoni A, Sacco A, Moschetta M, Reagan MR, et al. The sialyltransferase ST3GAL6 influences homing and survival in multiple myeloma. Blood. 2014; 124:1765–76.
Search in Google Scholar Back to article
Chang L-Y, Liang S-Y, Lu S-C, Tseng HC, Tsai H-Y, Tang C-J, et al. Molecular basis and role of Siglec-7 ligand expression on chronic lymphocytic leukemia B cells. Front Immunol. 2022; 13:840388. doi: 10.3389/fimmu.2022.840388
Open DOI Search in Google Scholar Back to article
Miyagi T. Aberrant expression of sialidase and cancer progression. Proc Jpn Acad Ser B Phys Biol Sci. 2008; 84:407–18.
Search in Google Scholar Back to article
Topham NJ, Hewitt EW. Natural killer cell cytotoxicity: how do they pull the trigger? Immunology. 2009; 128:7–15.
Search in Google Scholar Back to article
Paust S, Senman B, von Andrian UH. Adaptive immune responses mediated by natural killer cells. Immunol Rev. 2010; 235:286–96.
Search in Google Scholar Back to article
Shao J-Y, Yin W-W, Zhang Q-F, Liu Q, Peng M-L, Hu H-D, et al. Siglec-7 defines a highly functional natural killer cell subset and inhibits cell-mediated activities. Scand J Immunol. 2016; 84:182–90.
Search in Google Scholar Back to article
Lübbers J, Rodríguez E, van Kooyk Y. Modulation of immune tolerance via Siglec-sialic acid interactions. Front Immunol. 2018; 9:2807. doi: 10.3389/fimmu.2018.02807
Open DOI Search in Google Scholar Back to article
Varchetta S, Mele D, Oliviero B, Mantovani S, Ludovisi S, Cerino A, et al. Unique immunological profile in patients with COVID-19. Cell Mol Immunol. 2021; 18:604–12.
Search in Google Scholar Back to article
Häuselmann I, Borsig L. Altered tumor-cell glycosylation promotes metastasis. Front Oncol. 2014; 4:28. doi: 10.3389/fonc.2014.00028
Open DOI Search in Google Scholar Back to article
Yang H, Lu L, Chen X. An overview and future prospects of sialic acids. Biotechnol Adv. 2021; 46:107678. doi: 10.1016/j.biotechadv.2020.107678
Open DOI Search in Google Scholar Back to article
Fuster MM, Esko JD. The sweet and sour of cancer: glycans as novel therapeutic targets. Nat Rev Cancer. 2005; 5:526–42.
Search in Google Scholar Back to article
Kajander T, Lehtinen MJ, Hyvärinen S, Bhattacharjee A, Leung E, Isenman DE, et al. Dual interaction of factor H with C3d and glycosaminoglycans in host-nonhost discrimination by complement. Proc Natl Acad Sci U S A. 2011; 108:2897–902.
Search in Google Scholar Back to article
Kim Y-H, Min KH, Wang Z, Kim J, Jacobson O, Huang P, et al. Development of sialic acid-coated nanoparticles for targeting cancer and efficient evasion of the immune system. Theranostics. 2017; 7:962–73.
Search in Google Scholar Back to article
Chen Z, Yu M, Guo L, Zhang B, Liu S, Zhang W, et al. Tumor derived SIGLEC family genes may play roles in tumor genesis, progression, and immune microenvironment regulation. Front Oncol. 2020; 10:586820. doi: 10.3389/fonc.2020.586820
Open DOI Search in Google Scholar Back to article
Huang P-J, Low P-Y, Wang I, Hsu S-TD, Angata T. Soluble Siglec-14 glycan-recognition protein is generated by alternative splicing and suppresses myeloid inflammatory responses. J Biol Chem. 2018; 293:19645–58.
Search in Google Scholar Back to article
Wang J, Sun J, Liu LN, Flies DB, Nie X, Toki M, et al. Siglec-15 as an immune suppressor and potential target for normalization cancer immunotherapy. Nat Med. 2019; 25:656–66.
Search in Google Scholar Back to article
Cao G, Xiao Z, Yin Z. Normalization cancer immunotherapy: blocking Siglec-15! Signal Transduct Target Ther. 2019; 4:10. doi: 10.1038/s41392-019-0045-x
Open DOI Search in Google Scholar Back to article
Liu Y, Li X, Zhang C, Zhang H, Huang Y. LINC00973 is involved in cancer immune suppression through positive regulation of Siglec-15 in clear-cell renal cell carcinoma. Cancer Sci. 2020; 111:3693–704. doi: 10.1111/cas.14611
Open DOI Search in Google Scholar Back to article
Udagawa N, Koide M, Nakamura M, Nakamichi Y, Yamashita T, Uehara S, et al. Osteoclast differentiation by RANKL and OPG signaling pathways. J Bone Miner Metab. 2021; 39:19–26.
Search in Google Scholar Back to article
Kohnz RA, Roberts LS, DeTomaso D, Bideyan L, Yan P, Bandyopadhyay S, et al. Protein sialylation regulates a gene expression signature that promotes breast cancer cell pathogenicity. ACS Chem Biol. 2016; 11:2131–9.
Search in Google Scholar Back to article
Teoh ST, Ogrodzinski MP, Ross C, Hunter KW, Lunt SY. Sialic acid metabolism: a key player in breast cancer metastasis revealed by metabolomics. Front Oncol. 2018; 8:174. doi: 10.3389/fonc.2018.00174
Open DOI Search in Google Scholar Back to article
van den Bijgaart RJE, Kroesen M, Wassink M, Brok IC, Kers-Rebel ED, Boon L, et al. Combined sialic acid and histone deacetylase (HDAC) inhibitor treatment up-regulates the neuroblastoma antigen GD2. J Biol Chem. 2019; 294:4437–49.
Search in Google Scholar Back to article
Büll C, Heise T, Beurskens DMH, Riemersma M, Ashikov A, Rutjes FPJT, et al. Sialic acid glycoengineering using an unnatural sialic acid for the detection of sialoglycan biosynthesis defects and on-cell synthesis of Siglec ligands. ACS Chem Biol. 2015; 10:2353–63.
Search in Google Scholar Back to article
Büll C, Boltje TJ, Balneger N, Weischer SM, Wassink M, van Gemst JJ, et al. Sialic acid blockade suppresses tumor growth by enhancing T-cell-mediated tumor immunity. Cancer Res. 2018; 78:3574–88.
Search in Google Scholar Back to article
Nakamura K, Terai Y, Tanabe A, Ono YJ, Hayashi M, Maeda K, et al. CD24 expression is a marker for predicting clinical outcome and regulates the epithelial-mesenchymal transition in ovarian cancer via both the Akt and ERK pathways. Oncol Rep. 2017;37:3189–200.
Search in Google Scholar Back to article
Kristiansen G, Winzer K-J, Mayordomo E, Bellach J, Schlüns K, Denkert C, et al. CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res. 2003; 9:4906–13.
Search in Google Scholar Back to article
Barkal AA, Brewer RE, Markovic M, Kowarsky M, Barkal SA, Zaro BW, et al. CD24 signalling through macrophage Siglec-10 is a target for cancer immunotherapy. Nature. 2019; 572(7769):392–6.
Search in Google Scholar Back to article
Abolhasani S, Shahbazloo SV, Saadati HM, Mahmoodi N, Khanbabaei N. Evaluation of serum levels of inflammation, fibrinolysis and oxidative stress markers in coronary artery disease prediction: a cross-sectional study. Arq Bras Cardiol. 2019; 113:667–74. [article in English and Portuguese]
Search in Google Scholar Back to article
Bakri RS, Afzali B, Covic A, Sriskantharan R, Bharma-Ariza P, Park WH, et al. Cardiovascular disease in renal allograft recipients is associated with elevated sialic acid or markers of inflammation. Clin Transplant. 2004; 18:201–4.
Search in Google Scholar Back to article
Christ ER, Cummings MH, Lumb PJ, Crook MA, Sönksen PH, Russell-Jones DL. Growth hormone (GH) replacement therapy reduces serum sialic acid concentrations in adults with GH-deficiency: a double-blind placebo-controlled study. Clin Endocrinol (Oxf). 1999; 51:173–9.
Search in Google Scholar Back to article
Masuda H, Wakabayashi R, Wakabayashi I. Serum sialic acid and ankle versus brachial arterial-pressure ratio in NIDDM. Scand J Clin Lab Invest. 1998; 58:433–39.
Search in Google Scholar Back to article
Zhang L, Wei T-T, Li Y, Li J, Fan Y, Huang F-Q, et al. Functional metabolomics characterizes a key role for N-acetylneuraminic acid in coronary artery diseases. Circulation. 2018; 137:1374–90.
Search in Google Scholar Back to article
Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, et al. Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation. 2003; 107:499–511.
Search in Google Scholar Back to article
Nigam PK, Narain VS, Kumar A. Sialic acid in cardiovascular diseases. Indian J Clin Biochem. 2006; 21:54–61.
Search in Google Scholar Back to article
Baumann H, Gauldie J. The acute phase response. Immunol Today. 1994; 15:74–80.
Search in Google Scholar Back to article
Romero R, Lens XM, Novoa D, Arcocha V, Alonso R, Arza MD, et al. Sialic acid is a predictor of cardiovascular complications in renal transplantation recipients. Nephron. 1993; 65:489–90.
Search in Google Scholar Back to article
Ogasawara Y, Namai T, Yoshino F, Lee M-C-i, Ishii K. Sialic acid is an essential moiety of mucin as a hydroxyl radical scavenger. FEBS Lett. 2007; 581:2473–7.
Search in Google Scholar Back to article
Tertov VV, Sobenin IA, Orekhov AN. Characterization of desialylated low-density lipoproteins which cause intracellular lipid accumulation. Int J Tissue React. 1992; 14:155–62.
Search in Google Scholar Back to article
Knuiman MW, Watts GF, Divitini ML. Is sialic acid an independent risk factor for cardiovascular disease? A 17-year follow-up study in Busselton, Western Australia. Ann Epidemiol. 2004; 14:627–32.
Search in Google Scholar Back to article
Prajna K, Kumar JA, Rai S, Shetty SK, Rai T, Shrinidhi, et al. Predictive value of serum sialic acid in type-2 diabetes mellitus and its complication (nephropathy). J Clin Diagn Res. 2013; 7:2435–7. doi: 10.7860/jcdr/2013/6210.3567
Open DOI Search in Google Scholar Back to article
Nayak SB, Bhaktha G. Relationship between sialic acid and metabolic variables in Indian type 2 diabetic patients. Lipids Health Dis. 2005; 4:15. doi: 10.1186/1476-511x-4-15
Open DOI Search in Google Scholar Back to article
Varma V, Varma M, Varma A, Kumar R, Bharosay A, Vyas S. Serum total sialic acid and highly sensitive C-reactive protein: prognostic markers for the diabetic nephropathy. J Lab Physicians. 2016; 8:25–9. doi: 10.4103/0974-2727.176230
Open DOI Search in Google Scholar Back to article
Shivananda Nayak B, Duncan H, Lalloo S, Maraj K, Matmungal V, Matthews F, et al. Correlation of microalbumin and sialic acid with anthropometric variables in type 2 diabetic patients with and without nephropathy. Vasc Health Risk Manag. 2008; 4:243–7.
Search in Google Scholar Back to article
Animaw W, Seyoum Y. Increasing prevalence of diabetes mellitus in a developing country and its related factors. PLoS One. 2017; 12:e0187670. doi: 10.1371/journal.pone.0187670
Open DOI Search in Google Scholar Back to article
Rogers ME, Williams DT, Niththyananthan R, Rampling MW, Heslop KE, Johnston DG. Decrease in erythrocyte glycophorin sialic acid content is associated with increased erythrocyte aggregation in human diabetes. Clin Sci (Lond). 1992; 82:309–13.
Search in Google Scholar Back to article
Shahvali S, Shahesmaeili A, Sanjari M, Karami-Mohajeri S. The correlation between blood oxidative stress and sialic acid content in diabetic patients with nephropathy, hypertension, and hyperlipidemia. Diabetol Int. 2020; 11:19–26. doi: 10.1007/s13340-019-00395-9
Open DOI Search in Google Scholar Back to article
Freeze HH, Eklund EA, Ng BG, Patterson MC. Neurology of inherited glycosylation disorders. Lancet Neurol. 2012; 11:453–66.
Search in Google Scholar Back to article
Siddiqui SS, Matar R, Merheb M, Hodeify R, Vazhappilly CG, Marton J, et al. Siglecs in brain function and neurological disorders. Cells. 2019; 8:1125. doi: 10.3390/cells8101125
Open DOI Search in Google Scholar Back to article
Schnaar RL, Gerardy-Schahn R, Hildebrandt H. Sialic acids in the brain: gangliosides and polysialic acid in nervous system development, stability, disease, and regeneration. Physiol Rev. 2014; 94:461–518.
Search in Google Scholar Back to article
Wielgat P, Walesiuk A, Braszko JJ. Effects of chronic stress and corticosterone on sialidase activity in the rat hippocampus. Behav Brain Res. 2011; 222:363–7.
Search in Google Scholar Back to article
Boyzo A, Ayala J, Gutiérrez R, Hernández-RJ. Neuraminidase activity in different regions of the seizing epileptic and non-epileptic brain. Brain Res. 2003; 964:211–7.
Search in Google Scholar Back to article
Minami A, Meguro Y, Ishibashi S, Ishii A, Shiratori M, Sai S, et al. Rapid regulation of sialidase activity in response to neural activity and sialic acid removal during memory processing in rat hippocampus. J Biol Chem. 2017; 292:5645–54.
Search in Google Scholar Back to article
Minami A, Ishii A, Shimba S, Kano T, Fujioka E, Sai S, et al. Down-regulation of glutamate release from hippocampal neurons by sialidase. J Biochem. 2018; 163:273–80.
Search in Google Scholar Back to article
Annunziata I, Patterson A, Helton D, Hu H, Moshiach S, Gomero E, et al. Lysosomal NEU1 deficiency affects amyloid precursor protein levels and amyloid-β secretion via deregulated lysosomal exocytosis. Nat Commun. 2013; 4:2734. doi: 10.1038/ncomms3734
Open DOI Search in Google Scholar Back to article
Schneider JS, Seyfried TN, Choi H-S, Kidd SK. Intraventricular sialidase administration enhances GM1 ganglioside expression and is partially neuroprotective in a mouse model of Parkinson's disease. PLoS One. 2015; 10:e0143351. doi: 10.1371/journal.pone.0143351
Open DOI Search in Google Scholar Back to article
De Palma M, Biziato D, Petrova TV. Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer. 2017; 17:457–74.
Search in Google Scholar Back to article
Chiodelli P, Urbinati C, Paiardi G, Monti E, Rusnati M. Sialic acid as a target for the development of novel antiangiogenic strategies. Future Med Chem. 2018; 10:2835–54.
Search in Google Scholar Back to article
Szabo R, Skropeta D. Advancement of sialyltransferase inhibitors: therapeutic challenges and opportunities. Med Res Rev. 2017; 37:219–70.
Search in Google Scholar Back to article
Elgohary MM, Helmy MW, Abdelfattah E-ZA, Ragab DM, Mortada SM, Fang J-Y, Elzoghby AO. Targeting sialic acid residues on lung cancer cells by inhalable boronic acid-decorated albumin nanocomposites for combined chemo/herbal therapy. J Control Release. 2018; 285:230–43.
Search in Google Scholar Back to article
Wang X, Tang H, Wang C, Zhang J, Wu W, Jiang X. Phenylboronic acid-mediated tumor targeting of chitosan nanoparticles. Theranostics. 2016; 6:1378–92.
Search in Google Scholar Back to article
Wang J, Wu W, Zhang Y, Wang X, Qian H, Liu B, Jiang X. The combined effects of size and surface chemistry on the accumulation of boronic acid-rich protein nanoparticles in tumors. Biomaterials. 2014; 35:866–78.
Search in Google Scholar Back to article
Tian H, Liu Q, Qin S, Zong C, Zhang Y, Yao S, et al. Synthesis and cardiovascular protective effects of quercetin 7-O-sialic acid. J Cell Mol Med. 2017; 21:107–20.
Search in Google Scholar Back to article
Xu X-L, Li W-S, Wang X-J, Du Y-L, Kang X-Q, Hu J-B, et al. Endogenous sialic acid-engineered micelles: a multifunctional platform for on-demand methotrexate delivery and bone repair of rheumatoid arthritis. Nanoscale. 2018; 10:2923–35.
Search in Google Scholar Back to article
Zhu M-L, Xu X-L, Wang X-J, Zhang N-N, Lu K-J, Qi J, et al. Sialic-acid-anchored micelles: a hierarchical targeting device for enhanced tumor tissue accumulation and cellular internalization. Mol Pharm. 2018; 15:4235–46.
Search in Google Scholar Back to article
Lin C-H, Yeh Y-C, Yang KD. Functions and therapeutic targets of Siglec-mediated infections, inflammations and cancers. J Formos Med Assoc. 2021; 120:5–24.
Search in Google Scholar Back to article
Khairnar A, Sunsunwal S, Babu P, Ramya TNC. Novel serine/threonine-O-glycosylation with N-acetylneuraminic acid and 3-deoxy-D-manno-octulosonic acid by bacterial flagellin glycosyltransferases. Glycobiology. 2021; 31:288–306.
Search in Google Scholar Back to article
King AMQ, Adams MJ, Lefkowitz E, Carstens EB, editors. Virus taxonomy: classification and nomenclature of viruses. Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier Academic Press; 2011, p. 1327.
Search in Google Scholar Back to article
Herrler G, Klenk HD. Structure and function of the HEF glycoprotein of influenza C virus. Adv Virus Res. 1991; 40:213–34.
Search in Google Scholar Back to article
Rosenberg A, editor. Biology of the sialic acids. New York: Springer Science; 1995.
Search in Google Scholar Back to article
Hellebø A, Vilas U, Falk K, Vlasak R. Infectious salmon anemia virus specifically binds to and hydrolyzes 4-O-acetylated sialic acids. J Virol. 2004; 78:3055–62.
Search in Google Scholar Back to article
Falk K, Aspehaug V, Vlasak R, Endresen C. Identification and characterization of viral structural proteins of infectious salmon anemia virus. J Virol. 2004; 78:3063–71.
Search in Google Scholar Back to article
Schultze B, Krempl C, Ballesteros ML, Shaw L, Schauer R, Enjuanes L, Herrler G. Transmissible gastroenteritis coronavirus, but not the related porcine respiratory coronavirus, has a sialic acid (N-glycolylneuraminic acid) binding activity. J Virol. 1996; 70:5634–7.
Search in Google Scholar Back to article
Noda M, Koide F, Asagi M, Inaba Y. Physicochemical properties of transmissible gastroenteritis virus hemagglutinin. Arch Virol. 1988; 99:163–72.
Search in Google Scholar Back to article
Schultze B, Herrler G. Bovine coronavirus uses N-acetyl-9-O-acetylneuraminic acid as a receptor determinant to initiate the infection of cultured cells. J Gen Virol. 1992; 73(Pt 4):901–6.
Search in Google Scholar Back to article
Li B, Wang L, Ge H, Zhang X, Ren P, Guo Y, et al. Identification of potential binding sites of sialic acids on the RBD domain of SARS-CoV-2 spike protein. Front Chem. 2021; 9:659764. doi: 10.3389/fchem.2021.659764
Open DOI Search in Google Scholar Back to article
Winter C, Schwegmann-Weßels C, Cavanagh D, Neumann U, Herrler G. Sialic acid is a receptor determinant for infection of cells by avian Infectious bronchitis virus. J Gen Virol. 2006; 87(Pt 5): 1209–16.
Search in Google Scholar Back to article
Sherman MB, Williams AN, Smith HQ, Nelson C, Wilen CB, Fremont DH, et al. Bile salts alter the mouse norovirus capsid conformation: possible implications for cell attachment and immune evasion. J Virol. 2019; 93:e00970–19. doi: 10.1128/jvi.00970-19
Open DOI Search in Google Scholar Back to article
Taube S, Perry JW, Yetming K, Patel SP, Auble H, Shu L, et al. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J Virol. 2009; 83:4092–101.
Search in Google Scholar Back to article
Alexander DA, Dimock K. Sialic acid functions in enterovirus 70 binding and infection. J Virol. 2002; 76:11265–72.
Search in Google Scholar Back to article
Nokhbeh MR, Hazra S, Alexander DA, Khan A, McAllister M, Suuronen EJ, et al. Enterovirus 70 binds to different glycoconjugates containing α2,3-linked sialic acid on different cell lines. J Virol. 2005; 79:7087–94.
Search in Google Scholar Back to article
Dukhinova M, Veremeyko T, Yung AWY, Kuznetsova IS, Lau TYB, Kopeikina E, et al. Fresh evidence for major brain gangliosides as a target for the treatment of Alzheimer's disease. Neurobiol Aging. 2019; 77:128–43.
Search in Google Scholar Back to article
Ding J, Sui D, Liu M, Su Y, Wang Y, Liu M, et al. Sialic acid conjugate-modified liposomes enable tumor homing of epirubicin via neutrophil/monocyte infiltration for tumor therapy. Acta Biomater. 2021; 134:702–15.
Search in Google Scholar Back to article
Sun J, Tian Q, Liu M, Su Y, Liu X, Deng Y, et al. Evaluation of the antitumor effect and immune response of micelles modified with a polysialic acid-d-α-tocopheryl polyethylene glycol 1000 succinate conjugate. AAPS PharmSciTech. 2021; 22:223. doi: 10.1208/s12249-021-02047-1
Open DOI Search in Google Scholar Back to article
Xu Q, Shan Y, Wang N, Liu Y, Zhang M, Ma M. Sialic acid involves in the interaction between ovomucin and hemagglutinin and influences the antiviral activity of ovomucin. Int J Biol Macromol. 2018; 119:533–9.
Search in Google Scholar Back to article
Wang X-J, Shu G-F, Xu X-L, Peng C-H, Lu C-Y, Cheng X-Y, et al. Combinational protective therapy for spinal cord injury medicated by sialic acid-driven and polyethylene glycol based micelles. Biomaterials. 2019; 217:119326. doi: 10.1016/j.biomaterials.2019.119326
Open DOI Search in Google Scholar Back to article
Morozzi C, Sedláková J, Serpi M, Avigliano M, Carbajo R, Sandoval L, et al. Targeting GNE myopathy: a dual prodrug approach for the delivery of N-acetylmannosamine 6-phosphate. J Med Chem. 2019; 62:8178–93.
Search in Google Scholar Back to article
Lai X, Wang S, Hu M, Sun Y, Chen M, Liu M, et al. Dual targeting single arrow: neutrophil-targeted sialic acid-modified nanoplatform for treating comorbid tumors and rheumatoid arthritis. Int J Pharm. 2021; 607:121022. doi: 10.1016/j.ijpharm.2021.121022
Open DOI Search in Google Scholar Back to article
Svennerholm L. Quantitative estimation of sialic acids. II. A colorimetric resorcinol-hydrochloric acid method. Biochim Biophys Acta. 1957; 24:604–11.
Search in Google Scholar Back to article
Warren L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959; 234:1971–5.
Search in Google Scholar Back to article
Roboz J, Suttajit M, Bekesi JG. Elimination of 2-deoxyribose interference in the thiobarbituric acid determination of N-acetylneuraminic acid in tumor cells by pH-dependent extraction with cyclohexanone. Anal Biochem. 1981; 110:380–8.
Search in Google Scholar Back to article
Durand G, Feger J, Coignoux M, Agneray J, Pays M. Rapid estimation of small amounts of formaldehyde liberated during periodate oxidation of a sialoglycoprotein. Anal Biochem. 1974; 61:232–6.
Search in Google Scholar Back to article
Massamiri Y, Durand G, Richard A, Féger J, Agneray J. Determination of erythrocyte surface sialic acid residues by a new colorimetric method. Anal Biochem. 1979; 97:346–51.
Search in Google Scholar Back to article
Yao K, Ubuka T. Determination of sialic acids by acidic ninhydrin reaction. Acta Med Okayama. 1987; 41:237–41.
Search in Google Scholar Back to article
Yao K, Ubuka T, Masuoka N, Kinuta M, Ikeda T. Direct determination of bound sialic acids in sialoglycoproteins by acidic ninhydrin reaction. Anal Biochem. 1989; 179:332–5.
Search in Google Scholar Back to article
Mudd AT, Salcedo J, Alexander LS, Johnson SK, Getty CM, Chichlowski M, et al. Porcine milk oligosaccharides and sialic acid concentrations vary throughout lactation. Front Nutr. 2016; 3:39. doi: 10.3389/fnut.2016.00039
Open DOI Search in Google Scholar Back to article
Sugahara K, Sugimoto K, Nomura O, Usui T. Enzymatic assay of serum sialic acid. Clin Chim Acta. 1980; 108:493–8.
Search in Google Scholar Back to article
Taniuchi K, Chifu K, Hayashi N, Nakamachi Y, Yamaguchi N, Miyamoto Y, et al. A new enzymatic method for the determination of sialic acid in serum and its application for a marker of acute phase reactants. Kobe J Med Sci. 1981; 27:91–102.
Search in Google Scholar Back to article
Li W, Liu Y, Zheng X, Gao J, Wang L, Li Y. Investigation of the potential use of sialic acid as a biomarker for rheumatoid arthritis. Ann Clin Lab Sci. 2019; 49:224–31.
Search in Google Scholar Back to article
Hernández-Arteaga AC, de Jesús Zermeño-Nava J, Martínez-Martínez MU, Hernández-Cedillo A, Ojeda-Galván HJ, José-Yacamán M, Navarro-Contreras HR. Determination of salivary sialic acid through nanotechnology: a useful biomarker for the screening of breast cancer. Arch Med Res. 2019; 50:105–10.
Search in Google Scholar Back to article
Zermeño-Nava JJ, Martínez-Martínez MU, Rámirez-de-Ávila AL, Hernández-Arteaga AC, García-Valdivieso MG, Hernández-Cedillo A, et al. Determination of sialic acid in saliva by means of surface-enhanced Raman spectroscopy as a marker in adnexal mass patients: ovarian cancer vs benign cases. J Ovarian Res. 2018; 11:61. doi: 10.1186/s13048-018-0433-9
Open DOI Search in Google Scholar Back to article
Sun Y, Sun C, Zhang E. Expression of serum sialic acid, early antigen-IgA, and viral capsid antigen-IgA in nasopharynx cancer patients: the diagnostic implication of combined assays. Med Sci Monit. 2015; 21:4068–73.
Search in Google Scholar Back to article
Haroun RA, Osman WH, Eessa AM. Evaluation of serum total sialic acid in moderate COVID-19 patients with and without gastrointestinal tract manifestations. Tissue Cell. 2022; 74:101679. doi: 10.1016/j.tice.2021.101679
Open DOI Search in Google Scholar Back to article
Rasool M, Khan SR, Malik A, Khan KM, Zahid S, Manan A, et al. Comparative studies of salivary and blood sialic acid, lipid peroxidation and antioxidative status in oral squamous cell carcinoma (OSCC). Pak J Med Sci. 2014; 30:466–71.
Search in Google Scholar Back to article

Sialic acid: an attractive biomarker with promising biomedical applications

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