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Although well characterized in humans, it is less known for birds. Studies have reported the identification of several \u03b1 subunits along with the presence of endogenous cofactors in different avian erythrocytes. However, the native structure of avian hemoglobin remains elusive. Native top-down mass spectrometry (nTD-MS) offers powerful insights into biomolecular complexes, providing information on quaternary structure, subunit connectivity, stoichiometry, and subunit sequences. However, most nTD-MS approaches use direct infusion, which can limit the multiprotein complex population characterization. Here, we report on the development of a size-exclusion-chromatography (SEC) nTD-MS approach, including different activation methods to characterize the zebra finch hemoglobin structure. Three different tetramer populations were separated and characterized using optimized pMS2 (pseudo-MS2, complex-up) workflows to induce subunit and endogenous cofactor release previously reported by our group. The analytical strategy was improved with the addition of an extra level of characterization through the implementation of a pMS3 (pseudo-MS3, complex-down) step with controlled pressure, allowing almost complete sequence coverage of all the subunits (&amp;gt;94%), along with the identification of inositol pentaphosphate as a cofactor of the tetramer structure. Altogether, these results pinpoint the key role of SEC-nTD-MS workflows to enable a complete structural characterization of hemoglobin complexes, which could provide crucial information regarding oxygen affinity, bird environment adaptation, or phylogeny.<\/jats:p>","DOI":"10.1021\/jasms.6c00041","type":"journal-article","created":{"date-parts":[[2026,6,19]],"date-time":"2026-06-19T06:59:00Z","timestamp":1781852340000},"page":"2060-2071","source":"Crossref","is-referenced-by-count":0,"title":["Linkage between Quaternary Structure and Subunit Sequencing\nof Zebra Finch Hemoglobin via Hyphenation of Size Exclusion Chromatography\nwith Native Top-Down Mass Spectrometry"],"prefix":"10.1021","volume":"37","author":[{"given":"Le\u0301a","family":"Letissier","sequence":"first","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Corentin","family":"Beaumal","sequence":"additional","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Turkan","family":"Nabiyeva","sequence":"additional","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Franc\u0327ois","family":"Criscuolo","sequence":"additional","affiliation":[{"name":"Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5510-4868","authenticated-orcid":true,"given":"Fabrice","family":"Bertile","sequence":"additional","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christine","family":"Schaeffer-Reiss","sequence":"additional","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4013-4129","authenticated-orcid":true,"given":"Sarah","family":"Cianfe\u0301rani","sequence":"additional","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5524-4983","authenticated-orcid":true,"given":"Oscar","family":"Hernandez-Alba","sequence":"additional","affiliation":[{"name":"IPHC UMR 7178, Universite\u0301 de Strasbourg , , ,","place":["Strasbourg, France, CNRS 67087"]},{"name":"Infrastructure Nationale de Prote\u0301omique ProFI \u2212 ,","place":["Strasbourg, France, UAR2048 67087"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,6,19]]},"reference":[{"issue":"3","key":"2026090311505297900_cit1","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1016\/j.cell.2023.12.017","article-title":"Understanding\nthe Cell: Future Views of Structural Biology","volume":"187","author":"Beck","year":"2024","journal-title":"Cell"},{"issue":"6","key":"2026090311505297900_cit2","doi-asserted-by":"publisher","first-page":"542","DOI":"10.1056\/NEJMcp1103643","article-title":"Clinical\nPractice. Diagnosis of Diabetes","volume":"367","author":"Inzucchi","year":"2012","journal-title":"N. Engl. J.\nMed."},{"issue":"4","key":"2026090311505297900_cit3","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1016\/j.cbpb.2011.07.006","article-title":"Glucosensing\nand Glucose Homeostasis:\nFrom Fish to Mammals","volume":"160","author":"Polakof","year":"2011","journal-title":"Comp Biochem Physiol B\nBiochem Mol. Biol."},{"issue":"9442","key":"2026090311505297900_cit4","doi-asserted-by":"publisher","first-page":"1343","DOI":"10.1016\/S0140-6736(04)17192-4","article-title":"Sickle-Cell Disease","volume":"364","author":"Stuart","year":"2004","journal-title":"Lancet"},{"issue":"6","key":"2026090311505297900_cit5","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.1016\/j.cell.2013.05.039","article-title":"The Hallmarks\nof Aging","volume":"153","author":"Lo\u0301pez-Oti\u0301n","year":"2013","journal-title":"Cell"},{"issue":"10","key":"2026090311505297900_cit6","doi-asserted-by":"publisher","first-page":"2861","DOI":"10.1002\/prot.23112","article-title":"A Survey of Hemoglobin Quaternary\nStructures","volume":"79","author":"Dey","year":"2011","journal-title":"Proteins Struct. Funct. Bioinforma."},{"issue":"5273","key":"2026090311505297900_cit7","doi-asserted-by":"publisher","first-page":"726","DOI":"10.1038\/228726a0","article-title":"Stereochemistry\nof Cooperative Effects in Haemoglobin: Haem\u2013Haem Interaction\nand the Problem of Allostery","volume":"228","author":"Perutz","year":"1970","journal-title":"Nature"},{"issue":"2","key":"2026090311505297900_cit8","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/0022-2836(84)90472-8","article-title":"The Crystal Structure\nof Human Deoxyhaemoglobin at 1.74 \u00c5 Resolution","volume":"175","author":"Fermi","year":"1984","journal-title":"J. Mol. Biol."},{"issue":"19","key":"2026090311505297900_cit9","doi-asserted-by":"publisher","first-page":"6089","DOI":"10.1046\/j.1432-1327.2000.01699.x","article-title":"Structural\nand Functional Analysis of the Two Haemoglobins of the Antarctic Seabird Catharacta Maccormicki: Characterization of an Additional\nPhosphate Binding Site by Molecular Modelling","volume":"267","author":"Tamburrini","year":"2000","journal-title":"Eur. J. Biochem."},{"issue":"2","key":"2026090311505297900_cit10","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1515\/bchm3.1989.370.2.1197","article-title":"Amino-Acid Sequences and Functional\nDifferentiation\nof Hemoglobins A and D from Swift(Apus Apus,Apodiformes)","volume":"370","author":"Nothum","year":"1989","journal-title":"Biol. Chem. Hoppe. Seyler"},{"issue":"11","key":"2026090311505297900_cit11","doi-asserted-by":"publisher","first-page":"1875","DOI":"10.1007\/s13361-015-1185-z","article-title":"Top-down-Assisted\nBottom-up Method for Homologous Protein Sequencing: Hemoglobin from\n33 Bird Species","volume":"26","author":"Song","year":"2015","journal-title":"J. Am. Soc. Mass Spectrom."},{"issue":"23","key":"2026090311505297900_cit12","doi-asserted-by":"publisher","first-page":"12038","DOI":"10.1016\/S0021-9258(19)86424-4","article-title":"The Interaction of\nInositol Pentaphosphate with the Hemoglobins of\nHighland and Lowland Geese","volume":"254","author":"Rollema","year":"1979","journal-title":"J. Biol. Chem."},{"issue":"2","key":"2026090311505297900_cit13","doi-asserted-by":"publisher","first-page":"379","DOI":"10.1111\/j.1432-1033.1975.tb21013.x","article-title":"The Interaction\nof Organic Phosphates with Human and Chicken Hemoglobin","volume":"60","author":"Brygier","year":"1975","journal-title":"Eur. J. Biochem."},{"issue":"1","key":"2026090311505297900_cit14","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1016\/s1096-4959(03)00077-0","article-title":"Analysis of\nHighly Phosphorylated Inositols in Avian and Crocodilian Erythrocytes","volume":"135","author":"Lui\u0301s Villar","year":"2003","journal-title":"Comp. Biochem. Physiol. B: Biochem. Mol. Biol."},{"key":"2026090311505297900_cit15","doi-asserted-by":"publisher","first-page":"111811","DOI":"10.1016\/j.exger.2022.111811","article-title":"Resistance to Glycation in the Zebra\nFinch: Mass Spectrometry-Based Analysis and Its Perspectives for Evolutionary\nStudies of Aging","volume":"164","author":"Brun","year":"2022","journal-title":"Exp. Gerontol."},{"issue":"1","key":"2026090311505297900_cit16","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1146\/annurev-biophys-092721-085421","article-title":"Native\nMass Spectrometry:\nRecent Progress and Remaining Challenges","volume":"51","author":"Karch","year":"2022","journal-title":"Annu.\nRev. Biophys."},{"issue":"8","key":"2026090311505297900_cit17","doi-asserted-by":"publisher","first-page":"7952","DOI":"10.1021\/acs.chemrev.1c00356","article-title":"Integration of Mass Spectrometry\nData for Structural Biology","volume":"122","author":"Britt","year":"2022","journal-title":"Chem. Rev."},{"issue":"4926","key":"2026090311505297900_cit18","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1126\/science.2675315","article-title":"Electrospray\nIonization for Mass Spectrometry of Large Biomolecules","volume":"246","author":"Fenn","year":"1989","journal-title":"Science"},{"issue":"20","key":"2026090311505297900_cit19","doi-asserted-by":"publisher","first-page":"2299","DOI":"10.1021\/ac00171a028","article-title":"Laser Desorption Ionization of Proteins with Molecular\nMasses Exceeding 10,000 Da","volume":"60","author":"Karas","year":"1988","journal-title":"Anal. Chem."},{"issue":"4","key":"2026090311505297900_cit20","doi-asserted-by":"publisher","first-page":"632","DOI":"10.1021\/jasms.4c00348","article-title":"Evolution of Mass\nSpectrometers for High m\/z Biological Ion Formation,\nTransmission, Analysis and Detection:\nA Personal Perspective","volume":"36","author":"Campuzano","year":"2025","journal-title":"J. Am. Soc. Mass Spectrom."},{"issue":"8","key":"2026090311505297900_cit21","doi-asserted-by":"publisher","first-page":"7269","DOI":"10.1021\/acs.chemrev.1c00212","article-title":"High-Resolution\nNative Mass Spectrometry","volume":"122","author":"Tamara","year":"2022","journal-title":"Chem. Rev."},{"issue":"1","key":"2026090311505297900_cit22","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1146\/annurev-biochem-081424-044501","article-title":"Membrane Protein\nComplexity Revealed Through Native Mass Spectrometry","volume":"94","author":"Lawrence","year":"2025","journal-title":"Annu. Rev. Biochem."},{"issue":"15","key":"2026090311505297900_cit23","doi-asserted-by":"publisher","first-page":"8189","DOI":"10.1021\/acs.analchem.5c01095","article-title":"Mass Determination\nof Filled and Empty AAV5 Particles Enabled by Nanoelectrospray Ionization\nand Proton Transfer Charge Reduction","volume":"97","author":"Pizzala","year":"2025","journal-title":"Anal.\nChem."},{"key":"2026090311505297900_cit24","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/bs.aivir.2019.07.003","article-title":"Structural Mass\nSpectrometry Goes Viral","volume-title":"Advances in Virus\nResearch","author":"Du\u0308lfer","year":"2019"},{"issue":"1","key":"2026090311505297900_cit25","doi-asserted-by":"publisher","first-page":"3610","DOI":"10.1038\/s41467-022-31029-5","article-title":"Sizing up DNA Nanostructure Assembly\nwith Native Mass Spectrometry and Ion Mobility","volume":"13","author":"Van Dyck","year":"2022","journal-title":"Nat. Commun."},{"issue":"8","key":"2026090311505297900_cit26","doi-asserted-by":"publisher","first-page":"7909","DOI":"10.1021\/acs.chemrev.1c00696","article-title":"Approaches to Heterogeneity\nin Native Mass Spectrometry","volume":"122","author":"Rolland","year":"2022","journal-title":"Chem. Rev."},{"issue":"2","key":"2026090311505297900_cit27","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1042\/EBC20220098","article-title":"Seeing the Complete\nPicture: Proteins in Top-down Mass\nSpectrometry","volume":"67","author":"Habeck","year":"2023","journal-title":"Essays Biochem."},{"issue":"7","key":"2026090311505297900_cit28","doi-asserted-by":"publisher","first-page":"1149","DOI":"10.1007\/s13361-019-02201-x","article-title":"Top or Middle? Up\nor Down? Toward a Standard Lexicon for Protein Top-Down and Allied\nMass Spectrometry Approaches","volume":"30","author":"Lermyte","year":"2019","journal-title":"J. Am. Soc. Mass\nSpectrom."},{"key":"2026090311505297900_cit29","doi-asserted-by":"publisher","first-page":"102180","DOI":"10.1016\/j.cbpa.2022.102180","article-title":"Deciphering\nCombinatorial Post-Translational Modifications by Top-down Mass Spectrometry","volume":"70","author":"Brodbelt","year":"2022","journal-title":"Curr. Opin. Chem. Biol."},{"issue":"7","key":"2026090311505297900_cit30","doi-asserted-by":"publisher","first-page":"100989","DOI":"10.1016\/j.mcpro.2025.100989","article-title":"Top-Down and Middle-Down\nMass Spectrometry of Antibodies","volume":"24","author":"Khristenko","year":"2025","journal-title":"Mol. Cell.\nProteomics"},{"key":"2026090311505297900_cit31","doi-asserted-by":"publisher","first-page":"784","DOI":"10.1021\/acs.analchem.2c02948","article-title":"Top-Down Ion Mobility\nSeparations of Isomeric Proteoforms","author":"Berthias","year":"2022","journal-title":"Anal. Chem."},{"issue":"17","key":"2026090311505297900_cit32","doi-asserted-by":"publisher","first-page":"9430","DOI":"10.1021\/acs.analchem.5c00705","article-title":"Ion Mobility\nGas-Phase Separation Enhances Top-Down Mass Spectrometry of Heavily\nModified Guide RNA","volume":"97","author":"Macias","year":"2025","journal-title":"Anal. Chem."},{"issue":"24","key":"2026090311505297900_cit33","doi-asserted-by":"publisher","first-page":"12746","DOI":"10.1021\/acs.analchem.5c01561","article-title":"Top-Down Characterization\nof Yeast tRNA by Gas-Phase Fractionation and Collisionally Activated\nDissociation Informed by Electron Photodetachment Charge Reduction\nMass Spectrometry","volume":"97","author":"Lanzillotti","year":"2025","journal-title":"Anal. Chem."},{"issue":"1","key":"2026090311505297900_cit34","doi-asserted-by":"publisher","first-page":"46","DOI":"10.1021\/pr034054u","article-title":"Affecting\nProton Mobility in Activated\nPeptide and Whole Protein Ions via Lysine Guanidination","volume":"3","author":"Pitteri","year":"2004","journal-title":"J. Proteome Res."},{"issue":"24","key":"2026090311505297900_cit35","doi-asserted-by":"publisher","first-page":"9347","DOI":"10.1021\/acs.analchem.3c01426","article-title":"Added Value of Internal\nFragments for Top-Down Mass Spectrometry of Intact Monoclonal Antibodies\nand Antibody\u2013Drug Conjugates","volume":"95","author":"Wei","year":"2023","journal-title":"Anal. Chem."},{"issue":"3\u20134","key":"2026090311505297900_cit36","doi-asserted-by":"publisher","DOI":"10.1002\/pmic.202300069","article-title":"Monitoring\nmAb Proteoforms in Mouse Plasma Using an\nAutomated Immunocapture Combined with Top-down and Middle-down Mass\nSpectrometry","volume":"24","author":"Dhenin","year":"2024","journal-title":"Proteomics"},{"issue":"5","key":"2026090311505297900_cit37","doi-asserted-by":"publisher","first-page":"1876","DOI":"10.1002\/mas.21793","article-title":"Native Top-down Mass Spectrometry\nfor Higher-order\nStructural Characterization of Proteins and Complexes","volume":"42","author":"Liu","year":"2023","journal-title":"Mass Spectrom. Rev."},{"issue":"48","key":"2026090311505297900_cit38","doi-asserted-by":"publisher","first-page":"12918","DOI":"10.1039\/D0SC04392C","article-title":"Higher-Order Structural Characterisation\nof Native Proteins and Complexes by Top-down Mass Spectrometry","volume":"11","author":"Zhou","year":"2020","journal-title":"Chem. Sci."},{"issue":"12","key":"2026090311505297900_cit39","doi-asserted-by":"publisher","first-page":"2388","DOI":"10.1038\/s41592-024-02279-6","article-title":"Top-down Mass Spectrometry of Native\nProteoforms and Their Complexes: A Community Study","volume":"21","author":"Habeck","year":"2024","journal-title":"Nat. Methods"},{"issue":"1","key":"2026090311505297900_cit40","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1038\/nchembio.2515","article-title":"Top-down\nCharacterization\nof Endogenous Protein Complexes with Native Proteomics","volume":"14","author":"Skinner","year":"2018","journal-title":"Nat. Chem. Biol."},{"issue":"14","key":"2026090311505297900_cit41","doi-asserted-by":"publisher","first-page":"1928","DOI":"10.1021\/acs.accounts.2c00216","article-title":"Native Mass Spectrometry at the Convergence\nof Structural Biology and Compositional Proteomics","volume":"55","author":"Joo\u00df","year":"2022","journal-title":"Acc. Chem. Res."},{"issue":"9","key":"2026090311505297900_cit42","doi-asserted-by":"publisher","first-page":"2197","DOI":"10.1021\/jasms.4c00224","article-title":"Characterization\nof a Monoclonal Antibody by Native and Denaturing Top-Down Mass Spectrometry","volume":"35","author":"Oates","year":"2024","journal-title":"J. Am. Soc. Mass Spectrom."},{"issue":"6","key":"2026090311505297900_cit43","doi-asserted-by":"publisher","first-page":"2491","DOI":"10.1021\/acs.analchem.3c04526","article-title":"Internal Fragments Enhance Middle-Down Mass Spectrometry\nStructural Characterization of Monoclonal Antibodies and Antibody-Drug\nConjugates","volume":"96","author":"Wei","year":"2024","journal-title":"Anal. Chem."},{"issue":"2","key":"2026090311505297900_cit44","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1038\/nchem.2908","article-title":"An Integrated Native\nMass Spectrometry and Top-down\nProteomics Method That Connects Sequence to Structure and Function\nof Macromolecular Complexes","volume":"10","author":"Li","year":"2018","journal-title":"Nat. Chem."},{"issue":"48","key":"2026090311505297900_cit45","doi-asserted-by":"publisher","first-page":"21826","DOI":"10.1021\/jacs.2c06726","article-title":"Native Top-Down\nMass Spectrometry with Collisionally Activated Dissociation Yields\nHigher-Order Structure Information for Protein Complexes","volume":"144","author":"Lantz","year":"2022","journal-title":"J. Am. Chem. Soc."},{"issue":"22","key":"2026090311505297900_cit46","doi-asserted-by":"publisher","first-page":"6610","DOI":"10.1039\/D2SC01536F","article-title":"Mapping Paratopes\nof Nanobodies Using Native Mass Spectrometry and Ultraviolet Photodissociation","volume":"13","author":"Macias","year":"2022","journal-title":"Chem. 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