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Microbiology (2000), 146, 2521-2530.
© 2000 Society for General Microbiology

Pseudomonas: Biology and Diversity

Secreted products of a nonmucoid Pseudomonas aeruginosa strain induce two modes of macrophage killing: external-ATP-dependent, P2Z-receptor-mediated necrosis and ATP-independent, caspase-mediated apoptosis

Olga Zaborina1, Neelam Dhiman1, Mei Ling Chen2, Jan Kostal1, Ian Alan Holder3 and Ananda M. Chakrabarty1

Dept of Microbiology & Immunology1 and Research Resource Center2, University of Illinois College of Medicine, 835 South Wolcott Avenue, Chicago, IL 60612, USA
Dept of Microbiology, Shriners Burns Hospital, 3229 Burnet Avenue, Cincinnati, OH 45229, USA3

Author for correspondence: Ananda M. Chakrabarty. Tel:+1 312 996 4586. Fax:+1 312 996 6415. e-mail: Ananda.Chakrabarty{at}uic.edu

A nonmucoid clinical isolate of Pseudomonas aeruginosa, strain 808, elaborated ATP-dependent and ATP-independent types of cytotoxic factors in the growth medium. These cytotoxic factors, active against macrophages, were secreted during the exponential phase of growth in a complex medium. Commensurate with the appearance of the cytotoxic activities in the cell-free growth medium, several ATP-utilizing enzymic activities, such as adenylate kinase, nucleoside diphosphate kinase and 5'-nucleotidase (ATPase and/or phosphatase), were detected in the medium. These ATP-utilizing enzymes are believed to convert external ATP, presumably effluxed from macrophages, to various adenine nucleotides, which then activate purinergic receptors such as P2Z, leading to enhanced macrophage cell death. Pretreatment of macrophages with periodate-oxidized ATP (oATP), which is an irreversible inhibitor of P2Z receptor activation, prevented subsequent ATP-induced macrophage cell death. A second type of cytotoxic factor(s) operated in an ATP-independent manner such that it triggered activation of apoptotic processes in macrophages, leading to proteolytic conversion of procaspase-3 to active caspase-3. This cytotoxic factor(s) did not appear to act on procaspase-3 present in macrophage cytosolic extracts. Intact macrophages, when exposed to the cytotoxic factor(s) for 6–16 h, underwent apoptosis and demonstrated the presence of active caspase-3 in their cytosolic extracts. Interestingly, two redox proteins, azurin and cytochrome c551, were detected in the cytotoxic preparation. When cell-line-derived or peritoneal macrophages or mast cells were incubated overnight with Q-Sepharose column flow-through fraction or with a mixture of azurin and cytochrome c551, they underwent extensive cell death due to induction of apoptosis.

Keywords: ATP-utilizing enzymes, Pseudomonas aeruginosa virulence, programmed cell death, azurin, cytochrome c551

Abbreviations: Ak, adenylate kinase; CF, cystic fibrosis; LDH, lactate dehydrogenase; Ndk, nucleoside diphosphate kinase; oATP, oxidized ATP




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