Mycobacterium tuberculosis acquires iron by cell-surface sequestration and internalization of human holo-transferrin

Boradia, Vishant Mahendra; Malhotra, Himanshu; Thakkar, Janak Shrikant; Tillu, Vikas Ajit; Vuppala, Bhavana; Patil, Pravinkumar; Sheokand, Navdeep; Sharma, Prerna; Chauhan, Anoop Singh; Raje, Manoj; Raje, Chaaya Iyengar

doi:10.1038/ncomms5730

Cited by 109Tuberculosis Research and EpidemiologyIron Metabolism and DisordersBacterial Genetics and Biotechnology

Mycobacterium tuberculosis acquires iron by cell-surface sequestration and internalization of human holo-transferrin

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Boradia, Vishant Mahendra, Malhotra, Himanshu, Thakkar, Janak Shrikant, Tillu, Vikas Ajit, Vuppala, Bhavana, Patil, Pravinkumar, Sheokand, Navdeep, Sharma, Prerna +3 more·2014·Nature Communications

DOI 10.1038/ncomms5730

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Abstract

Mycobacterium tuberculosis (M.tb), which requires iron for survival, acquires this element by synthesizing iron-binding molecules known as siderophores and by recruiting a host iron-transport protein, transferrin, to the phagosome. The siderophores extract iron from transferrin and transport it into the bacterium. Here we describe an additional mechanism for iron acquisition, consisting of an M.tb protein that drives transport of human holo-transferrin into M.tb cells. The pathogenic strain M.tb H37Rv expresses several proteins that can bind human holo-transferrin. One of these proteins is the glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase (GAPDH, Rv1436), which is present on the surface of M.tb and its relative Mycobacterium smegmatis. Overexpression of GAPDH results in increased transferrin binding to M.tb cells and iron uptake. Human transferrin is internalized across the mycobacterial cell wall in a GAPDH-dependent manner within infected macrophages.

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Mycobacteria acquire iron through multiple avenues including acquisition from transferrin via the endocytic pathway, by directly binding iron-loaded transferrin via specific receptors, by uptake of cytoplasmic iron or heme iron by specific transporters, or by production of siderophores such as mycobactin.
“Mycobacteria acquire iron through multiple avenues including the acquisition of the metal from transferrin via the endocytic pathway, by directly binding iron-loaded transferrin via specific receptors, by uptake of cytoplasmic iron or heme iron by specific transporters, or by the production of siderophores such as mycobactin, which can bind iron and re-utilize the metal (174–177).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [176]

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Henderson, B. E., Fares, M. A., & Martin, A. C. R. (2016) · doi:10.1002/9781118952108.ch8

Host glyceraldehyde-3-phosphate dehydrogenase-mediated iron acquisition is hijacked by intraphagosomal Mycobacterium tuberculosis
Patidar, A., Malhotra, H., Chaudhary, S., Kumar, M., Dilawari, R., Chaubey, G. K., Dhiman, A., Modanwal, R., Talukdar, S., Raje, C. I., et al. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-04110-3 · Cited by 9 · see citing works
Self-citation
Mycobacterium tuberculosis Glyceraldehyde-3-Phosphate Dehydrogenase (GAPDH) Functions as a Receptor for Human Lactoferrin
Malhotra, H., Patidar, A., Boradia, V. M., Kumar, R., Nimbalkar, R. D., Kumar, A., Gani, Z., Kaur, R., Garg, P., Raje, M., et al. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00245 · Cited by 56 · see citing works
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Differentiating the roles of Mycobacterium tuberculosis substrate binding proteins, FecB and FecB2, in iron uptake
de Miranda, R., Cuthbert, B. J., Klevorn, T., Chao, A., Mendoza, J., Arbing, M. A., Sieminski, P. J., Papavinasasundaram, K. G., Abdul-Hafiz, S., Chan, S., et al. (2023) · PLoS Pathogens · doi:10.1371/journal.ppat.1011650 · Cited by 11 · see citing works
Intraphagosomal Mycobacterium tuberculosis Acquires Iron from Both Extracellular Transferrin and Intracellular Iron Pools
Olakanmi, O., Schlesinger, L. S., Ahmed, A., & Britigan, B. E. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m209768200 · Cited by 122 · see citing works
Iron uptake and transport by the carboxymycobactin-mycobactin siderophore machinery of Mycobacterium tuberculosis is dependent on the iron-regulated protein HupB
Choudhury, M., Koduru, T. N., Kumar, N., Salimi, S., Desai, K., Prabhu, N. P., & Sritharan, M. (2021) · BioMetals · doi:10.1007/s10534-021-00292-2 · Cited by 18 · see citing works

Authors: Boradia, V. M., Malhotra, H., Thakkar, J. S., Tillu, V. A., Vuppala, B., Patil, P., Sheokand, N., Sharma, P., Chauhan, A. S., Raje, M., & Raje, C. I.
Affiliations: National Institute of Pharmaceutical Education and Research (IN)
Institute of Microbial Technology (IN)
Corresponding author: Raje, Manoj
Raje, Chaaya Iyengar
ORCID: Boradia, Vishant Mahendra
Malhotra, Himanshu
Tillu, Vikas Ajit
Sharma, Prerna
Chauhan, Anoop Singh
Raje, Manoj
Raje, Chaaya Iyengar
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2014-08-28
Volume: 5
Issue: 1
Pages: 4730-4730
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/ncomms5730
OpenAlex: W1967490650
Cited by: 108
References: 61
Citations by year: 2026: 8 · 2025: 5 · 2024: 9 · 2023: 13 · 2022: 6 · 2021: 8 · 2020: 9 · 2019: 12 · 2018: 9 · 2017: 7 · 2016: 11 · 2015: 9 · 2014: 2
FWCI: 6.80
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Communications (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: Department of Biotechnology, Ministry of Science and Technology, India
Department of Science and Technology, Ministry of Science and Technology, India
Indian Institute of Science Education and Research Mohali
CSIR - Institute of Microbial Technology
Topics: Health Sciences › Medicine › Infectious Diseases › Tuberculosis Research and Epidemiology
Health Sciences › Medicine › Hematology › Iron Metabolism and Disorders
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
Keywords: Mycobacterium tuberculosis, iron acquisition, transferrin, glyceraldehyde-3-phosphate dehydrogenase, siderophores, phagosome, macrophages, protein internalization, host-pathogen interaction, Mycobacterium smegmatis
MeSH terms: Amino Acid Sequence, Animals, Bacterial Proteins, Cell Wall, Female, Humans, Iron, Macrophages, Mice, Inbred BALB C, Molecular Sequence Data, Mycobacterium tuberculosis, Rabbits, Transferrin, Siderophores, Mycobacterium smegmatis, Glyceraldehyde-3-Phosphate Dehydrogenase (Phosphorylating), Immunoprecipitation, Host-Pathogen Interactions

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Mycobacterium tuberculosis acquires iron by cell-surface sequestration and internalization of human holo-transferrin

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