Leishmania donovani Exploits Macrophage Heme Oxygenase-1 To Neutralize Oxidative Burst and TLR Signaling–Dependent Host Defense
Abstract
Screening of macrophage antioxidant enzymes during infection revealed marked upregulation of the heme-degrading enzyme, heme oxygenase-1 (HO-1). Moreover, HO-1-silenced RAW macrophages depicted increased superoxide production and decreased parasite survival. HO-1 induction decreased cellular heme content, thereby inhibiting the heme-dependent maturation of gp91phox, a catalytic component of major reactive oxygen species-producing enzyme NAD(P)H oxidase. Decreased gp91phox expression resulted in reduced stability of p22phox, another component of the catalytic center of NAD(P)H oxidase. Replenishing infected cells with exogenous heme reversed these effects and restored NAD(P)H oxidase activity. Persistent HO-1 expression at late hour of infection prompted us to investigate its effect on other host defense parameters, and inhibition study revealed a reciprocal relationship of HO-1 with host proinflammatory responses. Among all the HO-1-mediated heme degradation products (CO, Fe, and biliverdin), only CO documented potent anti-inflammatory effects. Quenching of CO during infection increased the production of disease-resolving cytokines IL-12 and TNF-α. Coimmunoprecipitation experiments revealed that CO inhibited the interaction of TLR4 with MyD88 and TIR domain-containing adapter-inducing IFN-β, thereby dampening the activation of NF-κB and IFN regulatory factor 3-mediated production of proinflammatory cytokines. Administration of HO-1 inhibitor tin protoporphyrin IX dichloride in infected BALB/c mice led to a decrease in liver and spleen parasite burden along with increased production of IL-12 and TNF-α. These results suggest that HO-1 on one hand inhibits reactive oxygen species generation and on the other hand downregulates host favorable cytokine responses, thereby facilitating intramacrophage parasite survival.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Leishmania induces HO1 for acquisition of molecular iron and for protection from host-mediated formation of antimicrobial radicals.
“In addition, Leishmania induces HO1 for acquisition of molecular iron and for protection from host-mediated formation of antimicrobial radicals (Saha et al., 2019).”
From Iron in infection and immunity (2020) · cites this paper as Saha et al., 2019
Cites
Akira, S., & Takeda, K. (2004) · Nature reviews. Immunology · doi:10.1038/nri1391 · Cited by 8,312 · see citing works
Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway
Otterbein, L. E., Bach, F. H., Alam, J., Soares, M., Tao Lu, H., Wysk, M., Davis, R. J., Flavell, R. A., & Choi, A. M. K. (2000) · Nature Medicine · doi:10.1038/74680 · Cited by 2,153 · see citing works
Reduced stress defense in heme oxygenase 1-deficient cells
Poss, K. D., & Tonegawa, S. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.20.10925 · Cited by 1,293 · see citing works
Monocyte-Mediated Defense Against Microbial Pathogens
Serbina, N. V., Jia, T., Hohl, T. M., & Pamer, E. G. (2008) · Annual Review of Immunology · doi:10.1146/annurev.immunol.26.021607.090326 · Cited by 1,116 · see citing works
Macrophage defense mechanisms against intracellular bacteria
Weiss, G., & Schaible, U. E. (2015) · Immunological Reviews · doi:10.1111/imr.12266 · Cited by 989 · see citing works
Motterlini, R., Foresti, R., Bassi, R., & Green, C. J. (2000) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(00)00294-x · Cited by 846 · see citing works
Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria
Pamplona, A., Ferreira, A., Balla, J., Jeney, V., Balla, G., Epiphanio, S., Chora, Â., Rodrigues, C. D., Gregoire, I. P., Cunha-Rodrigues, M., et al. (2007) · Nature Medicine · doi:10.1038/nm1586 · Cited by 560 · see citing works
Are Reactive Oxygen Species Always Detrimental to Pathogens?
Paiva, C. N., & Bozza, M. T. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5447 · Cited by 559 · see citing works
The NADPH oxidase of professional phagocytes—prototype of the NOX electron transport chain systems
Cross, A. R., & Segal, A. W. (2004) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2004.03.008 · Cited by 489 · see citing works
Nakahira, K., Kim, H. P., Geng, X. H., Nakao, A., Wang, X., Murase, N., Drain, P. F., Wang, X., Sasidhar, M., Nabel, E. G., et al. (2006) · The Journal of Experimental Medicine · doi:10.1084/jem.20060845 · Cited by 356 · see citing works
Chauveau, C., Remy, S., Royer, P., Hill, M., Tanguy‐Royer, S., Hubert, F., Tesson, L., Brion, R., Bériou, G., Grégoire, M., et al. (2005) · Blood · doi:10.1182/blood-2005-02-0494 · Cited by 342 · see citing works
Chung, S. W., Liu, X., Macias, A. A., Baron, R. M., & Perrella, M. A. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32730 · Cited by 325 · see citing works
Molecular composition and regulation of the Nox family NAD(P)H oxidases.
Sumimoto, H., Miyano, K., & Takeya, R. (2005) · Biochemical and Biophysical Research Communications - BBRC · doi:10.1016/j.bbrc.2005.08.210 · Cited by 314 · see citing works
Vinchi, F., Costa da Silva, M., Ingoglia, G., Petrillo, S., Brinkman, N., Zuercher, A., Cerwenka, A., Tolosano, E., & Muckenthaler, M. U. (2016) · Blood · doi:10.1182/blood-2015-08-663245 · Cited by 269 · see citing works
Missall, T. A., Lodge, J. K., & McEwen, J. E. (2004) · Eukaryotic Cell · doi:10.1128/ec.3.4.835-846.2004 · Cited by 223 · see citing works
Oxidative Stress and Induction of Heme Oxygenase-1 in the Kidney in Sickle Cell Disease
Nath, K. A., Grande, J. P., Haggard, J. J., Croatt, A. J., Katušić, Z. S., Solovey, A. N., & Hebbel, R. P. (2001) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64037-0 · Cited by 185 · see citing works
Taillé, C., Benna, J. E., Lanone, S., Dang, M.-C., Ogier‐Denis, É., Aubier, M., & Boczkowski, J. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310661200 · Cited by 181 · see citing works
Lee, I.-T., Luo, S., Lee, C., Wang, S., Lin, C., Chang, C., Chen, Y., Chau, L., & Yang, C. (2009) · American Journal Of Pathology · doi:10.2353/ajpath.2009.090016 · Cited by 177 · see citing works
Toll‐Like Receptor and Heme Oxygenase‐1 Signaling in Hepatic Ischemia/Reperfusion Injury
Shen, X., Ke, B., Zhai, Y., Gao, F., Busuttil, R. W., Cheng, G., & Kupiec‐Weglinski, J. W. (2005) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2005.00932.x · Cited by 171 · see citing works
Leishmania donovani lipophosphoglycan blocks NADPH oxidase assembly at the phagosome membrane
Lodge, R., Diallo, T. O., & Descoteaux, A. (2006) · Cellular Microbiology · doi:10.1111/j.1462-5822.2006.00758.x · Cited by 169 · see citing works
Esfandiari, N., Sharma, R., Saleh, R., Thomas, A., & Agarwal, A. (2003) · Journal of Andrology · doi:10.1002/j.1939-4640.2003.tb03137.x · Cited by 160 · see citing works
Matheoud, D., Moradin, N., Bellemare-Pelletier, A., Shio, M. T., Hong, W. J., Olivier, M., Gagnon, É., Desjardins, M., & Descoteaux, A. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.06.003 · Cited by 148 · see citing works
Heme Oxygenase-1 Is an Anti-Inflammatory Host Factor that Promotes Murine Plasmodium Liver Infection
Epiphânio, S., Mikolajczak, S. A., Gonçalves, L. A., Pamplona, A., Portugal, S., Albuquerque, S., Goldberg, M. S., Rebelo, S., Anderson, D. G., Akinc, A., et al. (2008) · Cell Host & Microbe · doi:10.1016/j.chom.2008.04.003 · Cited by 141 · see citing works
Ke, B., Buelow, R., Shen, X., Melinek, J., Amersi, F. F., Gao, F., Ritter, T., Volk, H., Busuttil, R. W., & Kupiec‐Weglinski, J. W. (2002) · Human Gene Therapy · doi:10.1089/104303402320138970 · Cited by 127 · see citing works
Das, L., Datta, N., Bandyopadhyay, S. K., & Das, P. K. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.6.4020 · Cited by 123 · see citing works
Segal, A. W. (2007) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2007.10.003 · Cited by 122 · see citing works
Carbon Monoxide Inhibits TLR-Induced Dendritic Cell Immunogenicity
Remy, S., Blancou, P., Tesson, L., Tardif, V., Brion, R., Royer, P., Motterlini, R., Foresti, R., Painchaut, M., Pogu, S., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0802436 · Cited by 120 · see citing works
Woo, K. J., Lee, T. J., Park, J., & Kwon, T. K. (2006) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2006.02.116 · Cited by 119 · see citing works
Kathirvel, E., Chen, P., Morgan, K., French, S. W., & Morgan, T. R. M. (2009) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2009.06196.x · Cited by 117 · see citing works
Role and effect of IL-2 in experimental visceral leishmaniasis.
Murray, H. W., Miralles, G. D., Stoeckle, M. Y., & McDermott, D. F. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.151.2.929 · Cited by 110 · see citing works
Cytoprotective role of heme oxygenase-1 and heme degradation derived end products in liver injury
Origassa, C. S. T., & Câmara, N. O. S. (2013) · World Journal of Hepatology · doi:10.4254/wjh.v5.i10.541 · Cited by 97 · see citing works
Ball, W. B., Kar, S., Mukherjee, M., Chande, A. G., Mukhopadhyaya, R., & Das, P. K. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1004237 · Cited by 97 · see citing works
Haem oxygenase‐1 dictates intrauterine fetal survival in mice via carbon monoxide
Zenclussen, M. L., Casalis, P. A., El‐Mousleh, T., Rebelo, S., Langwisch, S., Linzke, N., Volk, H., Fest, S., Soares, M. P., & Zenclussen, A. C. (2011) · The Journal of Pathology · doi:10.1002/path.2946 · Cited by 95 · see citing works
Role of haem oxygenase-1 in microbial host defence
Chung, S. W., Hall, S. R. R., & Perrella, M. A. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01261.x · Cited by 95 · see citing works
Heme Oxygenase-1 Promotes the Persistence of Leishmania chagasi Infection
Luz, N. F., Andrade, B. B., Feijó, D. F., Araújo-Santos, T., Carvalho, G. Q., Andrade, D., Abánades, D. R., de Melo, E. V., Silva, A. M., Brodskyn, C., et al. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1103072 · Cited by 89 · see citing works
Srivastav, S., Kar, S., Chande, A. G., Mukhopadhyaya, R., & Das, P. K. (2012) · The Journal of Immunology · doi:10.4049/jimmunol.1102845 · Cited by 85 · see citing works
Gupta, P., Srivastav, S., Saha, S., Das, P. K., & Ukil, A. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.101 · Cited by 84 · see citing works
Lodge, R., & Descoteaux, A. (2006) · European Journal of Immunology · doi:10.1002/eji.200636089 · Cited by 80 · see citing works
Biosynthesis of Flavocytochrome b 558
Yu, L., DeLeo, F. R., Biberstine-Kinkade, K. J., Renee, J., Nauseef, W. M., & Dinauer, M. C. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.7.4364 · Cited by 78 · see citing works
Marinissen, M. J., Tanos, T., Bolós, M., de Sagarra, M. R., Coso, O. A., & Cuadrado, A. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m512199200 · Cited by 77 · see citing works
Pham, N.-K., Mouriz, J., & Kima, P. E. (2005) · Infection and Immunity · doi:10.1128/iai.73.12.8322-8333.2005 · Cited by 76 · see citing works
Kim, H., So, H., Lee, J., Lee, J., Park, C., Park, S.-Y., Kim, Y., Youn, M., Kim, S.-J., Chung, S.-Y., et al. (2006) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2006.01.018 · Cited by 75 · see citing works
Leishmania Interferes with Host Cell Signaling to Devise a Survival Strategy
Bhardwaj, S., Srivastava, N., Sudan, R., & Saha, B. (2010) · BioMed Research International · doi:10.1155/2010/109189 · Cited by 72 · see citing works
Kar, S., Ukil, A., Sharma, G., & Das, P. K. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.0909644 · Cited by 65 · see citing works
Srivastav, S., Ball, W. B., Gupta, P., Giri, J., Ukil, A., & Das, P. K. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.496323 · Cited by 64 · see citing works
Mitterstiller, A.-M., Haschka, D., Dichtl, S., Nairz, M., Demetz, E., Talasz, H., Soares, M. P., Einwallner, E., Esterbauer, H., Fang, F. C., et al. (2016) · Cellular Microbiology · doi:10.1111/cmi.12578 · Cited by 62 · see citing works
Self-citationAbdalla, M. Y., Ahmad, I. M., Switzer, B., & Britigan, B. E. (2015) · Redox Biology · doi:10.1016/j.redox.2015.01.012 · Cited by 59 · see citing works
A New Role for Myeloid HO-1 in the Innate to Adaptive Crosstalk and Immune Homeostasis
Koliaraki, V., & Kollias, G. A. (2011) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-5632-3_9 · Cited by 40 · see citing works
Yamazaki, T., Kawai, C., Yamauchi, A., & Kuribayashi, F. (2011) · Tropical Medicine and Health · doi:10.2149/tmh.2011-08 · Cited by 38 · see citing works
HO-1 Protects against Hypoxia/Reoxygenation-Induced Mitochondrial Dysfunction in H9c2 Cardiomyocytes
Dongling, C., Jin, Z. X., Zhang, J., Jiang, L., Chen, K., He, X., Yinwei, S., Ke, J., & Wang, Y. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153587 · Cited by 35 · see citing works
Arsenescu, R. I., Blum, A. M., Metwali, A., Elliott, D. E., & Weinstock, J. V. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.7.3906 · Cited by 34 · see citing works
Apocynin: a potent NADPH oxidase inhibitor for the management of atrial fibrillation
Sovari, A. A., Morita, N., & Karagueuzian, H. S. (2008) · Redox Report · doi:10.1179/135100008x309000 · Cited by 30 · see citing works
Heme Oxygenase-1 and Carbon Monoxide Promote Burkholderia pseudomallei Infection
Stolt, C., Schmidt, I. H. E., Sayfart, Y., Steinmetz, I., & Bast, A. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1403104 · Cited by 21 · see citing works
Saha, A., Basu, M., & Ukil, A. (2018) · IUBMB Life · doi:10.1002/iub.1759 · Cited by 18 · see citing works
Bhunia, A. K., Sarkar, D., & Das, P. K. (1996) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.1996.tb05046.x · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Iron in infection and immunity
Nairz, M., & Weiss, G. (2020) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2020.100864 · Cited by 359 · see citing works
Bogdan, C. (2020) · Cytokine X · doi:10.1016/j.cytox.2020.100041 · Cited by 113 · see citing works
Mitochondrial Reactive Oxygen Species in Infection and Immunity
Mukherjee, A., Ghosh, K. K., Chakrabortty, S., Gulyás, B. Z., Padmanabhan, P., & Ball, W. B. (2024) · Biomolecules · doi:10.3390/biom14060670 · Cited by 92 · see citing works
The pathogenicity and virulence of Leishmania - interplay of virulence factors with host defenses
Gupta, A. K., Das, S., Kamran, M., Ejazi, S. A., & Ali, N. (2022) · Virulence · doi:10.1080/21505594.2022.2074130 · Cited by 74 · see citing works
Iron and Heme Metabolism at the Leishmania–Host Interface
Laranjeira‐Silva, M. F., Hamza, I., & Pérez-Victoria, J. M. (2020) · Trends in Parasitology · doi:10.1016/j.pt.2019.12.010 · Cited by 64 · see citing works
Host–Pathogen Interaction in Leishmaniasis: Immune Response and Vaccination Strategies
Yasmin, H., Adhikary, A., Al‐Ahdal, M. N., Roy, S., & Kishore, U. (2022) · Immuno · doi:10.3390/immuno2010015 · Cited by 61 · see citing works
Huang, B., Gui, M., An, H., Shen, J., Ye, F., Ni, Z., Zhan, H., Che, L., Lai, Z., Zeng, J., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115387 · Cited by 61 · see citing works
Costa, D. L., Amaral, E. P., Andrade, B. B., & Sher, A. (2020) · Antioxidants · doi:10.3390/antiox9121205 · Cited by 43 · see citing works
The clinical relevance of heme detoxification by the macrophage heme oxygenase system
Yeudall, S., Upchurch, C. M., & Leitinger, N. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1379967 · Cited by 36 · see citing works
Potential therapeutic targets shared between leishmaniasis and cancer
Rashidi, S., Fernández-Rubio, C., Manzano-Román, R., Mansouri, R., Shafiei, R., Ali‐Hassanzadeh, M., Barazesh, A., Karimazar, M., Hatam, G., & Nguewa, P. (2021) · Parasitology · doi:10.1017/s0031182021000160 · Cited by 34 · see citing works
Heme oxygenase-1 in protozoan infections: A tale of resistance and disease tolerance
Silva, R. C. M. C., Travassos, L. H., Paiva, C. N., & Bozza, M. T. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008599 · Cited by 32 · see citing works
How Severe Anaemia Might Influence the Risk of Invasive Bacterial Infections in African Children
Abuga, K. M., Muriuki, J. M., Williams, T. N., & Atkinson, S. H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21186976 · Cited by 30 · see citing works
Rizk, Y. S., Santos-Pereira, S., Gervazoni, L. F. O., Hardoim, D. D. J., Cardoso, F. D. O., de Souza, C. D. S. F., Pelajo‐Machado, M., Carollo, C. A., de Arruda, C. C. P., de Almeida-Amaral, E. E., et al. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.615814 · Cited by 27 · see citing works
Karmakar, J., & Mandal, C. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.626110 · Cited by 26 · see citing works
Bioactivity of Natural Polyphenols as Antiparasitic Agents and their Biochemical Targets
Soto‐Sánchez, J. (2022) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557522666220404090429 · Cited by 26 · see citing works
Cytokines and Signaling Networks Regulating Disease Outcomes in Leishmaniasis
Saha, A., Roy, S., & Ukil, A. (2022) · Infection and Immunity · doi:10.1128/iai.00248-22 · Cited by 26 · see citing works
Pathological roles of macrophages in Leishmania infections
Goto, Y., & Mizobuchi, H. (2023) · Parasitology International · doi:10.1016/j.parint.2023.102738 · Cited by 25 · see citing works
Morimoto, A., Uchida, K., CHAMBERS, J. K., Sato, K., Hong, J., Sanjoba, C., Matsumoto, Y., Yamagishi, J., & Goto, Y. (2019) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0007816 · Cited by 24 · see citing works
Perea-Martínez, A., García‐Hernández, R., Manzano, J. I., & Gamarro, F. (2022) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.1c00513 · Cited by 23 · see citing works
Chaparro, V., Graber, T. E., Alain, T., & Jaramillo, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-10317-6 · Cited by 21 · see citing works
DeSouza-Vieira, T. S., Iniguez, E., Serafim, T. D., de Castro, W., Karmakar, S., Disotuar, M. M., Cecílio, P., Lacsina, J. R., Meneses, C., Nagata, B. M., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108317 · Cited by 22 · see citing works
Saha, S., Roy, S., Dutta, A., Jana, K., & Ukil, A. (2021) · Infection and Immunity · doi:10.1128/iai.00764-20 · Cited by 22 · see citing works
Helou, D. G., Mauras, A., Fasquelle, F., Lanza, J. S., Loiseau, P. M., Betbeder, D., & Cojean, S. (2021) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0009627 · Cited by 22 · see citing works
Blot, C., Lavernhe, M., Lugo‐Villarino, G., Coulson, K., Salon, M., Tertrais, M., Planès, R., Santoni, K., Authier, H., Jacquemin, G., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114720 · Cited by 21 · see citing works
de Menezes, J. P. B., Khouri, R., Oliveira, C. V. S., Petersen, A. L. D. O. A., de Almeida, T. F., Mendes, F. R. L., Rebouças, A. D. A. D., Lorentz, A. L., Luz, N. F., Lima, J. B., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01362 · Cited by 21 · see citing works
Heme synthesis through the life cycle of the heme auxotrophic parasite Leishmania major
Orrego, L. M., Cabello‐Donayre, M., Vargas, P., Martínez‐García, M., Sánchez, C., Pineda‐Molina, E., Jiménez, M., Molina, R., & Pérez-Victoria, J. M. (2019) · The FASEB Journal · doi:10.1096/fj.201901274rr · Cited by 21 · see citing works
Bichiou, H., Rabhi, S., Hamda, C. B., Bouabid, C., Belghith, M., Piquemal, D., Trentin, B., Rabhi, I., & Guizani-Tabbane, L. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.748738 · Cited by 20 · see citing works
Leishmania donovani Metacyclic Promastigotes Impair Phagosome Properties in Inflammatory Monocytes
Matte, C., Duque, G. A., & Descoteaux, A. (2021) · Infection and Immunity · doi:10.1128/iai.00009-21 · Cited by 18 · see citing works
Hepatocellular HO-1 mediated iNOS-induced hepatoprotection against liver ischemia reperfusion injury
Qiao, Y., Xiao, F., Li, W., Yu, M., Du, P., Fang, Z., & Sun, J. L. (2019) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2019.11.053 · Cited by 14 · see citing works
TLR Signaling on Protozoan and Helminthic Parasite Infection
Fouzder, C., Mukhuty, A., Das, S., & Chattopadhyay, D. (2019) · IntechOpen eBooks · doi:10.5772/intechopen.84711 · Cited by 12 · see citing works
Roy, S., Roy, S., Halder, S., Jana, K., & Ukil, A. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107366 · Cited by 8 · see citing works
MicroRNA-21 and microRNA-148a affects PTEN, NO and ROS in canine leishmaniasis
de Freitas, J. H., Bragato, J. P., Rebech, G. T., Costa, S. F., dos Santos, M. O., Soares, M. F., Eugênio, F. D. R., dos Santos, P. S. P., & de Lima, V. M. F. (2023) · Frontiers in Genetics · doi:10.3389/fgene.2023.1106496 · Cited by 6 · see citing works
Akand, S. K., Rahman, A., Masood, M., Tabrez, S. S. M., Jawed, J. J., Ahmed, M. Z., Akhter, Y., Haque, M. M., & Rub, A. (2025) · Microbial Pathogenesis · doi:10.1016/j.micpath.2025.108019 · Cited by 6 · see citing works
Heme and immunity: The heme oxygenase dichotomy
Perry, M., & Hamza, I. (2025) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2025.112844 · Cited by 5 · see citing works
Pessôa-Pereira, D., Scorza, B. M., Cyndari, K. I., Beasley, E. A., & Petersen, C. A. (2023) · Pathogens · doi:10.3390/pathogens12091128 · Cited by 4 · see citing works
García‐Hernández, R., Manzano, J. I., Perea-Martínez, A., & Gamarro, F. (2022) · OMICS A Journal of Integrative Biology · doi:10.1089/omi.2021.0185 · Cited by 4 · see citing works
Spectrophotometric Assessment of Heme Oxygenase-1 Activity in Leishmania-infected Macrophages
Basu, M., Saha, S., & Ukil, A. (2020) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3578 · Cited by 3 · see citing works
Gao, Q., Gao, Z., Su, M., Huang, Y. L., Zhang, C., Li, C., Zhan, H., Liu, B., & Zhou, X. (2023) · Stem Cells International · doi:10.1155/2023/8887091 · Cited by 2 · see citing works
Das, T., Brahmachari, P., & Ukil, A. (2025) · mBio · doi:10.1128/mbio.02581-25 · Cited by 2 · see citing works
Li, F.-R., Sun, Q., Wang, Q., Qu, L.-L., Li, Z.-H., Yi, Z., & Yang, B.-B. (2026) · Parasites & Vectors · doi:10.1186/s13071-026-07361-w · Cited by 2 · see citing works
Global Remodeling of Host Proteome in Response to Leishmania Infection
Reyaz, E., Puri, N., & Selvapandiyan, A. (2023) · ACS Infectious Diseases · doi:10.1021/acsinfecdis.3c00492 · Cited by 1 · see citing works
Role of Apoptosis in Parasitic Infections: Therapeutic Targets and Strategies
Das, T., Roy, S., Das, P. K., & Ukil, A. (2024) · Springer eBooks · doi:10.1007/978-981-97-7905-5_14
Borrelia, Leishmania, and Babesia: An Emerging Triad of Vector-Borne Co-Infections?
Piloto‐Sardiñas, E., Cano‐Argüelles, A. L., & Cabezas‐Cruz, A. (2025) · Pathogens · doi:10.3390/pathogens14010036
Zhang, S. (2024) · doi:10.70675/60a97388z3f39z4829zbe4ezd73224b4a333
More than malaria: Exploring Babesia, Leishmania and Trypanosoma in sickle cell disease
Bhosale, C. R., Morcos, Z. L., Escudero, A., Neupane, R., Kahook, Z., Miranda, G., Deehan, E., Gregg, R. K., & Potter, A. K. (2026) · Current Research in Parasitology and Vector-Borne Diseases · doi:10.1016/j.crpvbd.2026.100396
The multifaceted role of cAMP signalling in Leishmania pathogenesis and host immune modulation
Das, T., Brahmachari, P., Das, P. K., & Ukil, A. (2026) · Cellular Signalling · doi:10.1016/j.cellsig.2026.112682
Wang, H., Xu, Z., Tian, Y., Zhang, Y., Cheng, Z., & Wang, Y. (2026) · Advanced Science · doi:10.1002/advs.76829
- Authors
- Saha, S., Basu, M., Guin, S., Gupta, P., Mitterstiller, A.-M., Weiss, G., Jana, K., & Ukil, A.
- Affiliations
- University of Calcutta (IN)
- Jadavpur University (IN)
- Centre international de recherche sur le cancer (FR)
- Innsbruck Medical University (AT)
- Department of Internal Medicine II, Infectious Diseases, Immunology, Rheumatology, Pneumology, Medical University of Innsbruck , 69008 Innsbruck ,
- Bose Institute (IN)
- Corresponding author
- Saha, Shriya
- Basu, Moumita
- Ukil, Anindita
- ORCID
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2019-02-01
- Volume
- 202
- Issue
- 3
- Pages
- 827-840
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- OpenAlex
- W2907823975
- Cited by
- 47
- References
- 55
- Citations by year
- 2026: 4 · 2025: 4 · 2024: 6 · 2023: 6 · 2022: 7 · 2021: 7 · 2020: 8 · 2019: 5
- FWCI
- 1.78
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- World Health Organization
- Division of Graduate Education
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Heme Oxygenase-1 and Carbon Monoxide
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Research on Leishmaniasis Studies
- Health Sciences › Medicine › Infectious Diseases › Leprosy Research and Treatment
- Keywords
- Leishmania donovani, heme oxygenase-1, macrophages, respiratory burst, NADPH oxidase, gp91phox, p22phox, heme degradation, carbon monoxide, TLR4 signaling, MyD88, TIRAP, NF-κB, IL-12, TNF-α, tin protoporphyrin IX, parasite survival, host-parasite interactions, anti-inflammatory response
- MeSH terms
- RAW 264.7 Cells, NADPH Oxidase 2, Animals, Female, Host-Parasite Interactions, Leishmania donovani, Macrophages, Membrane Proteins, Mice, Inbred BALB C, Protoporphyrins, Signal Transduction, Up-Regulation, Cytokines, Respiratory Burst, NADPH Oxidases, Toll-Like Receptor 4, Mice, Heme Oxygenase-1, Parasite Load
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review