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10.3390/pathogens10121614
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Article

Structural Characterization of Haemophilus influenzae Enolase and Its Interaction with Human Plasminogen by In Silico and In Vitro Assays

by
Yesenia Osorio-Aguilar
1,
Maria Cristina Gonzalez-Vazquez
1,
Diana Elizabeth Hernandez-Ceron
2,†,
Patricia Lozano-Zarain
1,
Ygnacio Martinez-Laguna
1,
Cesar Raul Gonzalez-Bonilla
3,
Rosa del Carmen Rocha-Gracia
1 and
Alejandro Carabarin-Lima
1,4,*
1
Posgrado en Microbiología, Laboratorio de Microbiología Hospitalaria y de la Comunidad, Centro de Investigaciones en Ciencias Microbiológicas, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla 72570, Mexico
2
Licenciatura en Biomedicina, Facultad de Medicina, Benemérita Universidad Autónoma de Puebla, Puebla 72420, Mexico
3
Director de Investigación Educativa, Instituto de Salud para el Bienestar, Acapulco 39355, Mexico
4
Licenciatura en Biotecnología, Instituto de Ciencias, Benemérita Universidad Autónoma de Puebla, Puebla 72570, Mexico
*
Author to whom correspondence should be addressed.
†
RIP.
Pathogens 2021, 10(12), 1614; https://doi.org/10.3390/pathogens10121614
Submission received: 10 November 2021 / Revised: 3 December 2021 / Accepted: 7 December 2021 / Published: 10 December 2021
(This article belongs to the Section Bacterial Pathogens)
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Abstract

Haemophilus influenzae is the causal agent of invasive pediatric diseases, such as meningitis, epiglottitis, pneumonia, septic arthritis, pericarditis, cellulitis, and bacteremia (serotype b). Non-typeable H. influenzae (NTHi) strains are associated with localized infections, such as otitis media, conjunctivitis, sinusitis, bronchitis, and pneumonia, and can cause invasive diseases, such as as meningitis and sepsis in immunocompromised hosts. Enolase is a multifunctional protein and can act as a receptor for plasminogen, promoting its activation to plasmin, which leads to the degradation of components of the extracellular matrix, favoring host tissue invasion. In this study, using molecular docking, three important residues involved in plasminogen interaction through the plasminogen-binding motif (251EFYNKENGMYE262) were identified in non-typeable H. influenzae enolase (NTHiENO). Interaction with the human plasminogen kringle domains is conformationally stable due to the formation of four hydrogen bonds corresponding to enoTYR253-plgGLU1 (K2), enoTYR253-plgGLY310 (K3), and enoLYS255-plgARG471/enoGLU251-plgLYS468 (K5). On the other hand, in vitro assays, such as ELISA and far-western blot, showed that NTHiENO is a plasminogen-binding protein. The inhibition of this interaction using polyclonal anti-NTHiENO antibodies was significant. With these results, we can propose that NTHiENO–plasminogen interaction could be one of the mechanisms used by H. influenzae to adhere to and invade host cells.
Keywords: Haemophilus influenzae; enolase; plasminogen-binding protein; interaction; virulence factor Haemophilus influenzae; enolase; plasminogen-binding protein; interaction; virulence factor

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MDPI and ACS Style

Osorio-Aguilar, Y.; Gonzalez-Vazquez, M.C.; Hernandez-Ceron, D.E.; Lozano-Zarain, P.; Martinez-Laguna, Y.; Gonzalez-Bonilla, C.R.; Rocha-Gracia, R.d.C.; Carabarin-Lima, A. Structural Characterization of Haemophilus influenzae Enolase and Its Interaction with Human Plasminogen by In Silico and In Vitro Assays. Pathogens 2021, 10, 1614. https://doi.org/10.3390/pathogens10121614

AMA Style

Osorio-Aguilar Y, Gonzalez-Vazquez MC, Hernandez-Ceron DE, Lozano-Zarain P, Martinez-Laguna Y, Gonzalez-Bonilla CR, Rocha-Gracia RdC, Carabarin-Lima A. Structural Characterization of Haemophilus influenzae Enolase and Its Interaction with Human Plasminogen by In Silico and In Vitro Assays. Pathogens. 2021; 10(12):1614. https://doi.org/10.3390/pathogens10121614

Chicago/Turabian Style

Osorio-Aguilar, Yesenia, Maria Cristina Gonzalez-Vazquez, Diana Elizabeth Hernandez-Ceron, Patricia Lozano-Zarain, Ygnacio Martinez-Laguna, Cesar Raul Gonzalez-Bonilla, Rosa del Carmen Rocha-Gracia, and Alejandro Carabarin-Lima. 2021. "Structural Characterization of Haemophilus influenzae Enolase and Its Interaction with Human Plasminogen by In Silico and In Vitro Assays" Pathogens 10, no. 12: 1614. https://doi.org/10.3390/pathogens10121614

APA Style

Osorio-Aguilar, Y., Gonzalez-Vazquez, M. C., Hernandez-Ceron, D. E., Lozano-Zarain, P., Martinez-Laguna, Y., Gonzalez-Bonilla, C. R., Rocha-Gracia, R. d. C., & Carabarin-Lima, A. (2021). Structural Characterization of Haemophilus influenzae Enolase and Its Interaction with Human Plasminogen by In Silico and In Vitro Assays. Pathogens, 10(12), 1614. https://doi.org/10.3390/pathogens10121614

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