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Garozzo, D. N-Glycomics of Human Erythrocytes. Encyclopedia. Available online: https://encyclopedia.pub/entry/16503 (accessed on 27 July 2024).
Garozzo D. N-Glycomics of Human Erythrocytes. Encyclopedia. Available at: https://encyclopedia.pub/entry/16503. Accessed July 27, 2024.
Garozzo, Domenico. "N-Glycomics of Human Erythrocytes" Encyclopedia, https://encyclopedia.pub/entry/16503 (accessed July 27, 2024).
Garozzo, D. (2021, November 29). N-Glycomics of Human Erythrocytes. In Encyclopedia. https://encyclopedia.pub/entry/16503
Garozzo, Domenico. "N-Glycomics of Human Erythrocytes." Encyclopedia. Web. 29 November, 2021.
N-Glycomics of Human Erythrocytes
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This entry is adapted from the peer-reviewed paper 10.3390/ijms22158063

Glycosylation is a complex post-translational modification that conveys functional diversity to glycoconjugates. Cell surface glycosylation mediates several biological activities such as induction of the intracellular signaling pathway and pathogen recognition. Red blood cell (RBC) membrane N-glycans determine blood type and influence cell lifespan. Although several proteomic studies have been carried out, the glycosylation of RBC membrane proteins has not been systematically investigated.

red blood cells N-glycosylation MALDI-TOF ABO(H) blood groups

1. Introduction

The red blood cell (RBC), or erythrocyte, is the simplest human cell, as it does not have internal organelles, which are lost during the erythropoiesis process. RBCs develop in the bone marrow and have a life span of about 100–120 days before they are recycled by macrophages [1]. In the last decade, several studies were carried out to shed light on the biological function of RBC membrane proteins [2][3]. As a result, the erythrocyte membrane is one of the best-known membranes in terms of structure, function, and associated genetic disorders [4][5][6]. The RBC membrane mediates transport functions and provides the erythrocytes with their structural features of resilience and deformability [7].
Glycosylation is a post-translational modification characterized by the covalent linkage of oligosaccharides moieties (glycans) to form glycoconjugates. Glycans are conjugated to asparagine (N-glycan) or serine/threonine (O-glycans) residues to form glycoproteins. Protein glycans play important roles in biological function/activity, protein folding, and molecular recognition [8]. Glycans are also recognized by glycan-binding proteins with lectin activity on opposing cells, and these glycan-ligand interactions are responsible for many biological activities, including the induction of the intracellular signaling pathway and recognition of pathogens such as influenza virus [8][9].
Changes in N-linked glycosylation have long been associated with disease development, and acquired glycan modifications have been described in multifactorial diseases such as cancer [10][11], inflammation [12][13], neurodegeneration [14][15], and genetic diseases [16][17].
Human RBC protein glycosylation has not been systematically examined in its entirety yet [18], though previous studies investigated the two most abundant glycoproteins of the erythrocyte membrane, namely band 3 and glycophorin A (GPA) [19][20][21][22]. In human erythrocytes, band 3 and other red blood cell membrane proteins bear poly-N-acetyllactosamine (poly-LacNAc) extensions, acting as an antigen carrier during various stages of cell development and differentiation [18][19]. The ABO(H) antigens were found as terminal non-reducing epitopes of large complex RBC N-glycans [23][24] and also constitute distinctive traits of outer arm glycophorin N-linked structures at lower molecular masses [18][25]. They play crucial roles in transfusion medicine, determining the compatibility between blood donors and recipients, as well as in the development of several hemostasis-related genetic disorders, including cardiovascular diseases and thrombosis [26][27]. Furthermore, several studies have investigated the relationship between the ABO(H) blood group distribution and the occurrence of some infectious diseases, such as HIV, malaria, influenza [28][29][30][31][32][33], and, recently, the COVID-19 pandemic [34][35][36][37].
Although information on the biological roles of glycan-binding proteins is still rising, challenges remain in detecting and profiling known and novel cellular glycans structures, due to the vast heterogeneity of possible glycoprotein isoforms depending on the glycan occupancy of protein glycosylation sites (macroheterogeneity) and on the variety of the attached glycans (microheterogeneity). Macroheterogeneity is related to the site availability, enzyme kinetics, and substrate concentrations that regulate the N-glycan precursor assembly and its subsequent transfer to the protein in cytosol and endoplasmic reticulum, whereas microheterogeneity is associated with the N-glycan processing occurring in endoplasmic reticulum and Golgi [17]. In this context, mass spectrometry (MS) techniques have demonstrated their capability for the characterization of unknown glycans and the high-throughput analysis of known glycan structures, allowing individual glycoforms to be distinguished [38]. Advances in mass spectrometry, and in particular in matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) MS, have driven substantial progress in glycan analysis [39]. The eligibility of MALDI-TOF is established because of its ability to analyze complex mixtures of glycans from biological samples together with its high detection sensitivity, as exemplified by several glycomic studies [40][41][42].
Since RBCs are continuously replenished with glycosylated membrane proteins that can be isolated, purified, and readily available from blood samples, glycosylation analysis of erythrocyte membrane glycoproteins might be the key for the early detection of glyco-biomarkers for diagnostic and therapeutic purposes as well as for studying interaction mechanisms involved in recognition of pathogens. In the present study, we applied high-sensitivity MALDI TOF MS-based glycomic methodologies to the analysis of total N-glycans derived from human erythrocyte membrane proteins, with the aim to generate an N-glycosylation fingerprinting of RBC. In particular, the total N-glycome of healthy subjects with different ABO(H) blood groups is evaluated as the starting point for future investigations.

2. N-Glycomics of Human Erythrocytes

It applied a robust and widely used MS-based glycomic approach to the extensive N-glycan characterization of RBCs. Our MALDI-TOF data showed erythrocyte membrane glycoproteins holding in prevalence complex bisected N-glycans with core and antennary fucosylation and recurrent poly-LacNAc extensions, in accordance with earlier glycosylation studies on specific red blood cell membrane proteins. The previous characterization of RBCs’ N-glycoproteins has been limited to their main components, such as band 3 and GPA proteins [19][20][21][22][25]. Band 3 was found harboring a single N-linked oligosaccharide, with a branched structure varying in the number of repeating LacNAc units terminated with Gal, fucose (Fuc), or NeuAc [19][20], whereas GPA, a major glycophorin, has been reported to bear 15 O-glycans [43][44] and a single N-linked glycan, mostly a biantennary sialylated moiety with bisecting GlcNAc and outer arm fucosylation [21][22]. In the current study, the MALDI-TOF strategy allowed a broad characterization of the total RBC N-glycans released from band 3, GPA, and additional minor glycoproteins. It observed large N-glycan structures up to 9 kDa (see Supplementary Figures) as a result of the ad hoc developed MS strategy that led to a notable improvement in upper mass-range sensitivity and signal-to-noise ratio. Besides a predominant portion of complex highly processed structures, also found oligomannose and hybrid N-glycans. As glycan structures are generated in the compartmentalized Golgi, changes in the relative signals of all the observed RBC N-glycans could be used as a diagnostic tool for the detection of defects in glycosylation enzymes involved in early Golgi processing in glycosylation-related diseases [45][46][47][48]. However, only a few studies reported on the N-glycosylation of human erythrocyte membrane glycoproteins using MS techniques [45][49][50], mostly focusing on the characterization of glycans from band 3 membrane glycoprotein in congenital dyserythropoietic anemia type II (CDA II), also called hereditary erythroblastic multinuclearity with the positive acidified-serum test (HEMPAS) [45][49]. Fukuda et al. in 1987 developed a method based on fast-atom bombardment (FAB) MS [45], whereas Denecke et al. in 2008 [49] compared erythrocyte band 3 mass mapping from HEMPAS and from a control by MALDI-TOF MS following SDS-PAGE and lectin-binding strategies. Both these studies accordingly found the lack of the large oligosaccharide component bearing the poly-LacNAc branches and the prevalence of glycans at lower molecular mass (such as oligomannose and hybrid and truncated complex species) in the red blood cell band 3 glycoprotein from HEMPAS patients, suggesting a defective Golgi processing in erythroblasts [45][49].
RBC membrane N-glycans are particularly exposed to the external environment, supporting the pathogen recognition processes. For instance, the hemagglutination assay is based on the interaction between the hemagglutinin located on the surface of the human-adapted influenza virus and some specific sialylated glycans on the epithelial cells of the human upper respiratory tract, defined as the key initial step of the infection cycle [51]. Accordingly, agglutination of chicken RBCs (cRBCs) [52] has long been used in viral titer assays as well as to investigate glycan receptor binding sites and in the testing of vaccines’ effectiveness [53][54][55][56]. The structural characterization of cell surface N-glycans of cRBCs, revealed the presence of bi- and triantennary structures capped with both α2→3 and α2→6 linked NeuAc and the lack of lactosamine repeating units [52]. On the other hand, the human bronchial epithelial cells, which are the target of human-adapted influenza A viruses, show the predominance of α2→6 sialylated glycans with lactosamine repeats [57][58]. These data could explain some pitfalls of the agglutination assay based on cRBCs which may not be representative of the physiological receptor for human-adapted influenza strains. Our study may trigger future advanced MS-based structural analyses on glycans from human RBCs, providing important insights for improved applications in this field.
The applied MALDI-TOF MS and MS/MS strategy presented here allowed for the characterization of glycans bearing the ABO(H) blood group antigens which, like genetic factors, are involved in several hemostasis-related diseases [26][27] and in many infectious diseases [28][29][30][31][32][33]. Several shreds of evidence suggest that the ABO(H) blood group expression may influence the development and the progression of cardiovascular disease, thrombosis, and hemostasis disorders. In the last year, there has been a growing interest in studying the association between the ABO(H) blood group distribution and the dynamics of the COVID-19 pandemic [34][35][36][37]. Recently, Liu et al. [36] found a positive correlation between the occurrence of COVID-19 infection cases and the proportion of blood group A by analyzing the data from the official WHO database. These results agree with other previous studies [34][35], strongly suggesting a relationship between the distribution of blood groups and the SARS-CoV-2 infection. However, the underlying mechanisms have not yet been clarified and further investigation, also taking into account the glycan-binding specificity and the glycosylation features of the SARS-CoV-2 proteins, is highly needed.

3. Conclusions

Our developed MS strategy led to a considerable improvement in upper mass-range sensitivity and in signal-to-noise ratio, in addition to a significant increase in the resolution of MALDI-TOF mass spectra, allowing for a detailed mapping of human RBC N-glycans. Since RBCs have a relatively short lifespan, these analytical strategies could be used to study possible glycosylation changes that can occur during disease conditions, for the early detection of potential glyco-biomarkers. Most important, this developed strategy could be a useful tool to investigate the interaction mechanisms of pathogen recognition as well as the ABO(H) blood group-mediated response to viral infections, with special regard to SARS-CoV-2.

References

  1. Ji, P.; Murata-hori, M.; Lodish, H.F. Formation of mammalian erythrocytes: Chromatin condensation and enucleation. Trends Cell Biol. 2011, 21, 409–415.
  2. Goodman, S.R.; Kurdia, A.; Ammann, L.; Kakhniashvili, D.; Daescu, O. The human red blood cell proteome and interactome. Exp. Biol. Med. 2007, 232, 1391–1408.
  3. Bryk, A.H.; Wiśniewski, J.R. Quantitative Analysis of Human Red Blood Cell Proteome. J. Proteome Res. 2017, 16, 2752–2761.
  4. Phillips, D.R.; Morrison, M. The arrangement of Proteins in the human erythrocyte membrane. Biochem. Biophys. Res. Commun. 1970, 40, 284–289.
  5. De Oliveira, S.; Saldanha, C. An overview about erythrocyte membrane. Clin. Hemorheol. Microcirc. 2010, 44, 63–74.
  6. Delaunay, J. The molecular basis of hereditary red cell membrane disorders. Blood Rev. 2007, 21, 1–20.
  7. Hochmuth, R. Erythrocyte Membrane Elasticity and Viscosity. Annu. Rev. Physiol. 1987, 49, 209–219.
  8. Varki, A. Biological roles of glycans. Glycobiology 2017, 27, 3–49.
  9. Stevens, J.; Blixt, O.; Tumpey, T.M.; Taubenberger, J.K.; Paulson, J.C.; Wilson, I.A. Structure and Receptor Specificity of the Hemagglutin from an H5N1 Influenza Virus. Science 2006, 312, 404–410.
  10. Pinho, S.S.; Reis, C.A. Glycosylation in cancer: Mechanisms and clinical implications. Nat. Rev. Cancer 2015, 15, 540–555.
  11. Magalhães, A.; Duarte, H.O.; Reis, C.A. Aberrant Glycosylation in Cancer: A Novel Molecular Mechanism Controlling Metastasis. Cancer Cell 2017, 31, 733–735.
  12. Shade, K.T.C.; Anthony, R. Antibody Glycosylation and Inflammation. Antibodies 2013, 2, 392–414.
  13. Albrecht, S.; Unwin, L.; Muniyappa, M.; Rudd, P.M. Glycosylation as a marker for inflammatory arthritis. Cancer Biomark. 2014, 14, 17–28.
  14. Hwang, H.; Zhaang, J.; Chung, K.A.; Leverenz, J.B.; Zabetian, C.P.; Peskind, E.R.; Jankovic, J.; Su, Z.; Hancock, A.M.; Pan, C.; et al. Glycoproteomics in neurodegenerative diseases. Mass Spectrom. Rev. 2010, 29, 79–125.
  15. Palmigiano, A.; Barone, R.; Sturiale, L.; Sanfilippo, C.; Bua, R.O.; Romeo, D.A.; Messina, A.; Capuana, M.L.; Maci, T.; Le Pira, F.; et al. CSF N-glycoproteomics for early diagnosis in Alzheimer’s disease. J. Proteom. 2016, 131, 29–37.
  16. Jaeken, J. Congenital disorders of glycosylation. Ann. N. Y. Acad. Sci. 2010, 1214, 190–198.
  17. Barone, R.; Sturiale, L.; Garozzo, D. Mass spectrometry in the characterization of human genetic N-glycosylation defects. Mass Spectrom. Rev. 2009, 28, 517–542.
  18. Aoki, T. A Comprehensive Review of Our Current Understanding of Red Blood Cell (RBC) Glycoproteins. Membranes 2017, 7, 56.
  19. Fukuda, M.; Dell, A.; Oates, J.E.; Fukuda, M.N. Structure of Branched Lactosaminoglycan, the Carbohydrate Moiety of Band 3 Isolated from Adult Human Erythrocytes. J. Biol. Chem. 1984, 259, 8260–8273.
  20. Tsuji, T.; Irimura, T.; Osawa, T. The carbohydrate moiety of band 3 glycoprotein of human erythrocyte membranes. Structures of lower molecular weight oligosaccharides. J. Biol. Chem. 1981, 256, 10497–10502.
  21. Yoshima, H.; Furthmayr, H.; Kobata, A. Structures of the asparagine-linked sugar chains of glycophorin A. J. Biol. Chem. 1980, 255, 9713–9718.
  22. Irimura, T.; Tsuji, T.; Tagami, S.; Yamamoto, K.; Osawa, T. Structure of a Complex-Type Sugar Chain of Human Glycophorin A. Biochemistry 1981, 20, 560–566.
  23. Wilczynska, Z.; Miller-Podraza, H.; Koscielak, J. The contribution of different glycoconjugates to the total ABH blood group activity of human erythrocytes. FEBS Lett. 1980, 112, 277–279.
  24. Krusius, T.; Finne, J.; Rauvala, H. The Poly(glycosy1) Chains of Glycoproteins. Characterisation of a novel type of glycoprotein saccharides from human erythrocyte membrane. Eur. J. Biochem. 1978, 92, 289–300.
  25. Fredriksson, S.Å.; Podbielska, M.; Nilsson, B.; Lisowska, E.; Krotkiewski, H. ABH blood group antigens in N-glycan of human glycophorin A. Arch. Biochem. Biophys. 2010, 498, 127–135.
  26. Lee-Sundlov, M.M.; Stowell, S.R.; Hoffmeister, K.M. Multifaceted role of glycosylation in transfusion medicine, platelets, and red blood cells. J. Thromb. Haemost. 2020, 18, 1535–1547.
  27. Stowell, S.R.; Stowell, C.P. Biologic roles of the ABH and Lewis histo-blood group antigens part II: Thrombosis, cardiovascular disease and metabolism. Vox Sang. 2019, 114, 535–552.
  28. Siransy, L.K.; Nanga, Z.Y.; Zaba, F.S.; Tufa, N.Y.; Dasse, S.R. ABO/Rh Blood Groups and Risk of HIV Infection and Hepatitis B among Blood Donors of Abidjan, Côte D’Ivoire. Eur. J. Microbiol. Immunol. 2015, 5, 205–209.
  29. Degarege, A.; Gebrezgi, M.T.; Ibanez, G.; Wahlgren, M.; Madhivanan, P. Effect of the ABO blood group on susceptibility to severe malaria: A systematic review and meta-analysis. Blood Rev. 2019, 33, 53–62.
  30. Horby, P.; Nguyen, N.Y.; Dunstan, S.J.; Baillie, J.K. The role of host genetics in susceptibility to influenza: A systematic review. PLoS ONE 2012, 7, e0033180.
  31. Li, D.; Wang, M.; Qi, J.; Zhang, Q.; Wang, H.; Pang, L.; Sun, X.; Duan, Z. Human group A rotavirus P VP8 * specifically binds to A-type histo-blood group antigen. Virology 2021, 555, 56–63.
  32. Tyrrell, D.A.J.; Sparrow, P.; Beare, A.S. Relation between Blood Groups and Resistance to Infection with Influenza and some Picornaviruses. Nature 1968, 220, 819–820.
  33. Davison, G.M.; Hendrickse, H.L.; Matsha, T.E. Membrane Influence Human Immunodeficiency Virus Infection? Cells 2020, 9, 845.
  34. Wu, Y.; Feng, Z.; Li, P.; Yu, Q. Relationship between ABO blood group distribution and clinical characteristics in patients with COVID-19. Clin. Chim. Acta 2020, 509, 220–223.
  35. E Fernandes, T.D.S. Chaotic model for COVID-19 growth factor. Res. Biomed. Eng. 2020, 1–5.
  36. Liu, Y.; Häussinger, L.; Steinacker, J.M.; Dinse-Lambracht, A. Association between the dynamics of the COVID-19 epidemic and ABO blood type distribution. Epidemiol. Infect. 2021, 149, E19.
  37. Pendu, J.L.; Breiman, A.; Rocher, J.; Dion, M.; Ruvoën-Clouet, N. ABO Blood Types and COVID-19: Spurious, Anecdotal, or Truly Important Relationships? A Reasoned Review of Available Data. Viruses 2021, 13, 160.
  38. Harvey, D.J. Proteomic analysis of glycosylation: Structural determination of N- and O-linked glycans by mass spectrometry. Expert Rev. Proteom. 2005, 2, 87–101.
  39. Banazadeh, A.; Veillon, L.; Wooding, K.M.; Zabet, M. Recent Advances in Mass Spectrometric Analysis of Glycoproteins. Electrophoresis 2017, 38, 162–189.
  40. North, S.J.; von Gunten, S.; Antonopoulos, A.; Trollope, A.; MacGlashan, D.W., Jr.; Jang-lee, J.; Dell, A.; Metcalfe, D.D.; Kirshenbaum, A.S.; Bochner, B.S.; et al. Glycomic analysis of human mast cells, eosinophils and basophils. Glycobiology 2012, 22, 12–22.
  41. Walther, T.; Karamanska, R.; Chan, R.W.Y.; Chan, M.C.W.; Jia, N.; Air, G.; Hopton, C.; Wong, M.P.; Dell, A.; Peiris, J.S.M.; et al. Glycomic Analysis of Human Respiratory Tract Tissues and Correlation with Influenza Virus Infection. PLoS Pathog. 2013, 9, e1003223.
  42. Vreeker, G.C.M.; Bladergroen, M.R.; Nicolardi, S.; Mesker, W.E.; Tollenaar, R.A.E.M.; van der Burgt, Y.E.M.; Wuhrer, M. Dried blood spot N-glycome analysis by MALDI mass spectrometry. Talanta 2019, 205, 120104.
  43. Pisano, A.; Redmond, J.W.; Williams, K.L.; Gooley, A.A. Glycosylation sites identified by solid-phase edman degradation: O-linked glycosylation motifs on human glycophorin A. Glycobiology 1993, 3, 429–435.
  44. Zdebska, E.; Kościelak, J. A single-sample method for determination of carbohydrate and protein contents glycoprotein bands separated by sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Anal. Biochem. 1999, 275, 171–179.
  45. Fukuda, M.N.; Dell, A.; Scartezzinill, P. Primary Defect of Congenital Dyserythropoietic Anemia Type II. Failure in glycosylation of erythrocyte lactosaminoglycan proteins caused by lowered N-acetylglucosaminyltransferase II. J. Biol. Chem. 1987, 262, 7195–7206.
  46. Climer, L.K.; Dobretsov, M.; Lupashin, V. Defects in the COG complex and COG-related trafficking regulators affect neuronal Golgi function. Front. Neurosci. 2015, 9, 405.
  47. Palmigiano, A.; Bua, R.O.; Barone, R.; Rymen, D.; Régal, L.; Deconinck, N.; Dionisi-Vici, C.; Fung, C.W.; Garozzo, D.; Jaeken, J.; et al. MALDI-MS profiling of serum O-glycosylation and N-glycosylation in COG5-CDG. J. Mass Spectrom. 2017, 52, 372–377.
  48. Fukuda, M.N.; Masri, K.A.; Dell, A.; Thonar, E.J.; Klier, G.; Lowenthal, R.M. Defective glycosylation of erythrocyte membrane glycoconjugates in a level of membrane-bound form of galactosyltransferase. Blood 1989, 73, 1331–1339.
  49. Denecke, J.; Kranz, C.; Nimtz, M.; Conradt, H.S.; Brune, T.; Heimpel, H.; Marquardt, T. Characterization of the N-glycosylation phenotype of erythrocyte membrane proteins in congenital dyserythropoietic anemia type II (CDA II/HEMPAS). Glycoconj. J. 2008, 25, 375–382.
  50. Samanta, S.; Dutta, D.; Ghoshal, A.; Mukhopadhyay, S.; Saha, B.; Sundar, S.; Jarmalavicius, S.; Forgber, M.; Mandal, C.; Walden, P.; et al. Glycosylation of erythrocyte spectrin and its modification in visceral leishmaniasis. PLoS ONE 2011, 6, e0028169.
  51. Gamblin, S.J.; Haire, L.F.; Russell, R.J.; Stevens, D.J.; Xiao, B.; Ha, Y.; Vasisht, N.; Steinhauer, D.A.; Daniels, R.S.; Elliot, A.; et al. The Structure and Receptor Binding Properties of the 1918 Influenza Hemagglutinin. Science 2004, 303, 1838–1842.
  52. Aich, U.; Beckley, N.; Shriver, Z.; Raman, R.; Viswanathan, K. Glycomics-based analysis of chicken red blood cells provides insight into the selectivity of the viral agglutination assay. FEBS J. 2011, 278, 1699–1712.
  53. Klimov, A.; Balish, A.; Veguilla, V.; Sun, H.; Schiffer, J.; Lu, X.; Katz, J.M.; Hancock, K. Influenza Virus Titration, Antigenic Characterization, and Serological Methods for Antibody Detection. In Influenza Virus: Methods and Protocols; Humana Press: Totowa, NJ, USA, 2012; Volume 1, pp. 25–51. ISBN 978-1-61779-620-3.
  54. Nobusawa, E.; Ishihara, H.; Morishita, T.; Sato, K.; Nakajima, K. Change in receptor-binding specificity of recent human influenza A viruses (H3N2): A single amino acid change in hemagglutinin altered its recognition of sialyloligosaccharides. Virology 2000, 278, 587–596.
  55. Bull, P.C.; Lowe, B.S.; Kortok, M.; Molyneux, C.S.; Newbold, C.I.; Marsh, K. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med. 1998, 4, 358–360.
  56. Katz, J.M.; Hancock, K.; Xu, X. Serologic assays for influenza surveillance, diagnosis and vaccine evaluation. Expert Rev. Anti. Infect. Ther. 2011, 9, 669–683.
  57. Chandrasekaran, A.; Srinivasan, A.; Raman, R.; Viswanathan, K.; Raguram, S.; Tumpey, T.M.; Sasisekharan, V.; Sasisekharan, R. Glycan topology determines human adaptation of avian H5N1 virus hemagglutinin. Nat. Biotechnol. 2008, 26, 107–113.
  58. Srinivasan, A.; Viswanathan, K.; Raman, R.; Chandrasekaran, A.; Raguram, S.; Tumpey, T.M.; Sasisekharan, V.; Sasisekharan, R. Quantitative biochemical rationale for differences in transmissibility of 1918 pandemic influenza A viruses. Proc. Natl. Acad. Sci. USA 2008, 15, 2800–2805.
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