Pathogenic Fungi: Host Interactions and Emerging Strategies for Control
Chapter Abstracts

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Chapter 1: Host Recognition by Fungal Pathogens
Elaine Bignell, Tom Rogers and Ken Haynes

Abstract
Fungi are highly versatile organisms. Many are able to adapt to diverse environmental conditions with ease, mounting transcriptional and physiological responses to an altering environment within very short time frames. This chapter will assess current evidence to support the hypothesis that pathogenic fungi are able to recognise "a host". We will consider the general importance of such mechanisms and how they might function in a range of infection scenarios. For the purposes of this discussion, possible host recognition mechanisms will be categorised as either sensory or molecular. We will draw upon reports from the fields of both human and phyto-pathogenic fungi to ask whether? and how? fungal pathogens recognise the host.


Chapter 2: Virulence Factors that Protect the Fungus from Elimination
Marta Feldmesser

Abstract
Fungal pathogens must evade intricate host defences in order to produce disease. At present, few "classical" virulence factors have been defined that operate in this capacity. Comparatively more is known about the ways in which host defence is altered by Blastomyces dermatitidis BAD1 and Cryptococcus neoformans capsular polysaccharide and melanin. The ability to undergo phenotypic switching in vivo adds to the mechanisms by which C. neoformans may thwart host responses. Pigment production also may be important for Aspergillus fumigatus, although pksP may contribute to virulence through other mechanisms. Additional understanding of ways by which fungi are protected from elimination is obtained by the examination of phenotypes that indicate that subversion of the host's ability to mount protective immune responses has occurred. The virulence determinant CPB1 is required by Histoplasma capsulatum to evade intracellular killing, though other factors are involved in determining the outcome of the host-pathogen interaction in the phagosome. The ability to produce inhibitory prostaglandins or induce prostaglandin production by the host is another such phenotype, although one of which present knowledge is rudimentary. Examination of these virulence factors and phenotypes illustrates the complexity of the mechanisms that protect fungi from elimination by the host.


Chapter 3: Virulence factors That Promote Invasion of Candida albicans
Martin Schaller, Hans Christian Korting, and Bernhard Hube

Abstract
Candida albicans, a facultative pathogenic microorganism, has developed several virulence traits which facilitate invasion of host tissues and avoidance of host defence mechanisms. One group of virulence factors that contributes to this process are the hydrolytic enzymes which are extracellularly secreted by the fungus. The three most significant hydrolytic enzymes produced by C. albicans species are secreted aspartic proteinases (Sap), phospholipases (PL) and lipases (Lip). They may play a central role in the pathogenicity of candidiasis. Their hydrolytic activity likely has a number of possible functions in addition to the simple role of digesting molecules for nutrition. Saps as the best-studied member of this group of hydrolytic enzymes contribute to host tissue invasion by digesting or destroying cell membranes and by degrading host surface molecules. There is also some evidence that hydrolytic enzymes are able to attack cells and molecules of the host immune system to avoid or resist antimicrobial activity. High hydrolytic activity with broad substrate specificity has been found in several Candida species, and most notably C. albicans. This activity is attributed to multigene families with at least ten members for Saps and Lips and several members for phospholipase B. Distinct members of these gene families are differentially regulated in various Candida infections. In the future, prevention and control of Candida infections might be achieved by pharmacological or immunological tools specifically modulated to inhibit virulence factors, e.g. the family of secreted aspartic proteinases.


Chapter 4: Adaptation to Oxidative, Nutrient and pH Stress by Human Pathogenic Fungi
Neeraj Chauhan and Richard A. Calderone

Abstract
The human pathogenic fungi overcome numerous environmental stress conditions both outside and within the host that challenge their ability to grow. That they survive is primarily a function of their ability to transmit stress signals by signal transduction pathways that regulate their genomes to adapt to each stress condition. Adaptation of commensal fungi occurs at mucosal surfaces such as the gastrointestinal tract, the oral cavity or vaginal canal. Here, nutrient limitations, competitors, pH, and host factors exert their negative influences on the residing microbiota, including fungi. Environmentally acquired fungi that cause human disease also encounter both similar and dissimilar stress conditions that occur both within the host and in the environment. Likewise, these fungi must adapt or be eliminated. In this chapter, the adaptation of human pathogenic fungi to oxidant, pH, and nutritional stress is discussed. Oxidant stress is exerted by both the host and by the environment. Fungi utilize a number of mechanisms to overcome this barrier and resume their growth, including oxidant-degrading enzymes such as, catalase, peroxidase, and superoxide dismutase as well as melanin that acts as an oxidant-neutralizing biomolecule. Further, oxidants that are generated during metabolism of fungi (or by the host, conceivably) are neutralized by other enzymes that restore a reduced condition to the cellular physiology. Signal pathways that adapt cells to oxidant stress include the 2-component signal transduction. A second stress condition that in the host may play a significant role in preventing fungal growth is pH. For example, the pH of the human vaginal canal and ecological niches within a site such as the oral cavity are acidic. Studies on pH response pathways in human pathogens have been limited to Candida species, but there are striking similarities in the method in which Candida and the non-pathogens, Saccharomyces cerevisiae and Aspergillus nidulans, respond to pH extremes. Finally, we discuss the mechanisms whereby fungi adapt to various types of nutrient stress. Most response mechanisms to nutrient stress are processed by several signal pathways, including the cAMP-protein kinase A, Snf1 and the TOR pathways. Each is discussed below. The challenge of future studies is to demonstrate the significance of these response elements to the challenge of the host. In some cases, as with the 2-component signal transduction as well as the TOR pathway and pH response pathways, relationships to the establishment of disease are currently being studied.


Chapter 5: Innate Immunity to Fungi: The Art of Speed and Specificity
Luigina Romani

Abstract
In the past decade, a dramatic shift has occurred in our mechanistic understanding of innate immunity. Precisely, the appreciation that activation of the innate immune system initiates, amplifies and drives antigen-specific immune responses together with the identification of discrete cell types, specific receptors and the signalling pathways involved in the activation of innate immunity has provided a multitude of new targets for exploitation by the development of adjuvants for vaccines. It has became apparent that understanding how immune responses are activated will result in the construction of better vaccines and immunomodulatory strategies that are effective at eliciting acquired protective immunity to fungi. The model has brought dendritic cells to center stage as promising targets for immunotherapy intervention, and vaccine development and has shifted the emphasis from the "antigen" towards the "adjuvant". Thus, the promise of a fungal vaccine will demand an adjuvant capable of stimulating the appropriate type of immune response best tailored to combating an infection. This objective can be achieved by targeting and manipulating cells and pathways of the innate immune system.


Chapter 6: T And B Lymphocytes In Mucosal Candidiasis
Flavia De Bernardis, Maria Boccanera, Consuelo Amantini and Giorgio Santoni

Abstract
The majority of human Candida infections occur at mucosal surfaces. Mucosal candidiasis (oropharyngeal and vaginal) is almost invariably observed in acquired immune deficiency syndrome (AIDS) patients. Vulvovaginal candidiasis is a widespread, common disease affecting a large proportion of healthy women with some of them affected by recurrent often intractable forms of the disease. However, in contrast to systemic candidiasis, relatively little is known about the role of mucosal immunity in protection against Candida. Therefore, understanding the components of the host-fungus interaction at the mucosal level can lead to a better understanding of the pathogenesis of mucosal candidiasis and result in the optimization of preventive and therapeutic antifungal strategies. C. albicans is capable of colonizing and persisting on mucosal surfaces and also of stimulating mucosal responses. The transition from asymptomatic colonization to symptomatic candidiasis occurs in presence of factors that enhance Candida virulence and/or are a result of a loss of defense mechanisms. Both humoral and cellular factors have been suggested to confer protection.This review summarizes the salient features of immune responses to Candida at the mucosal level with emphasis on the T and B cells and molecular interaction involved in their regulation. It also focuses on the defense mechanisms characterized in several animal models of candidiasis. In fact, animal models have provided an important contribution to the study of various aspects of the host's immune response against C. albicans at the mucosal level.


Chapter 7: Immunomodulation and Immunoprotection in Fungal Infections: Humoral and Cellular Immune Responses
Luiz R. Travassos, Arturo Casadevall, and Carlos P. Taborda

Abstract
The immunomodulation and immunotherapy of fungal infections depend on the recognition of antigens that can elicit protective antibody responses and/or activate and induce proliferation of effector cells of the immune system mediated by cytokines and other soluble factors. Antibodies and cellular immune responses can be induced by a wide variety of antigens but only a few will be effective in the immunoprotection against systemic mycoses. Researchers in this area are, therefore, continuously engaged in seeking for new compounds that show promising results in the treatment of experimental infections. Antibodies are believed to have protective role in Candida albicans, Cryptococcus neoformans and Pneumocystis carinii infections but less so in other systemic mycoses. Mixtures of antibodies, however, may contain protective, nonprotective and disease enhancing types that should be sorted out for the host benefit. Quantitative aspects are also critical for the success of antibody therapy. Monoclonal antibodies with defined specificity are essential in these studies. Other fungal agents such as Blastomyces dermatitidis, Histoplasma capsulatum, Coccidioides immitis and Paracoccidioides brasiliensis express glycoprotein antigens that induce protective cell-mediated reactions. Such adaptive immunity runs in parallel with the innate immunity to control fungal infections. Adaptive immunity involves mainly T CD4+ lymphocytes of the Th-1 subtype, producing IFN-g. In experimental histoplasmosis T CD8+ cells have also a role in immunoprotection. In terms of human immunoprotection, promiscuous peptides (with degenerate binding to MHC class II molecules) are the ones to be looked for while trying to transpose the results obtained in the mouse to human patients.


Chapter 8: Genomic Instability, Recombination and Adaptation in Candida albicans
Germán Larriba

Abstract
There is growing evidence that Candida albicans can achieve phenotypic variability by genomic rearrangements. For years, gross chromosomal rearrangements, as those represented by variation in the electrophoretical karyotypes especially among clinical isolates, have been the most widely studied. The establishment of a direct correlation between karyotype and phenotype is difficult because a chromosomal translocation can result in a modification of many traits as many genes have changed their genomic environment and likely their expression patterns. However, specific aneuploidies have been unambiguously correlated with specific mutants. The ability of C. albicans to generate these alterations in karyotype is not surprising in light of the genome structure, in particular the high frequency of repetitive elements belonging to several categories, as well as the diploid condition of the organism. In addition to gross rearrangements, more subtle changes such as gene conversion with or without crossover, other types of homologous or illegitimate recombination, substitution of bases, minor deletions or additions, etc, may also create genomic variability by affecting a single gene or a reduced number of genes. Adaptive mutagenesis appears especially advantageous for C. albicans since it would facilitate a rapid adaptation to the adverse conditions present in the human host. In fact, the behavior of the organism towards stress as well as the nature and distribution of some repeats, such as those present in MRS or ALS7 support that concept. Genotypic changes through a sexual interchange of genetic information are potentially possible since a sexual cycle has been recently discovered in C. albicans. However, recombination between homolog chromosomes received from each parent has not been reported so far and, therefore, the variability could be restricted to new combinations of chromosomes. Prezygotic and postzygotic barriers seem to account for the apparent inability of C. albicans diploids to return to the haploid state or for a tetraploid to return to the diploid state using meiosis.


Chapter 9: Antifungal Drugs, Targets and Target Discovery
Dongmei Li and Richard Calderone

Abstract
Invasive fungal infections have become one of the leading causes of death among patients with aggressive hematological malignances, transplant recipients, and other immunocompromised patients such as those with Acquired Immunodeficiency Syndrome (AIDS). The emergence of various opportunistic fungal infections and, for several human fungal pathogens, the rapid development of drug resistance, has prompted the search for new broad-spectrum antifungal agents that are minimally toxic and unlikely to result in the development of resistance. Current choices include the polyenes, of which amphotericin B is the most commonly used for treating invasive fungal disease, as well as a nucleoside analogue (5-fluorocytosine), and the azoles. With the exception of 5-fluorocytosine, the polyenes and azoles act by interfering with the structural or functional integrity of the fungal plasma membrane. However, while the target for the polyenes is the fungal sterol ergosterol, the selective nature of amphotericin B is compromised since the compound also binds to human cholesterol. Thus, toxicity is an invariable consequence of patient management when this drug is used, and new therapies are sought to avoid this problem. The azoles represent an impressive line of drugs that have found use in treating both superficial and invasive fungal disease that also cause fewer side effects than amphotericin B. However, there are problems with toxicity (ketoconazole, itraconazole), resistance, especially among the non-Candida albicans species of Candida (fluconazole), and a lack of efficacy against other important pathogens (Aspergillus fumigatus, fluconazole). The specificity of fungal cell wall targets has been exploited in the development of the b-1,3-glucan inhibitor caspofungin. Other drugs, either experimental or in clinical trials, include those that target unique fungal components, such as nikkomycins (chitin synthesis inhibitors), pradamicins, allylamines, sordarins and cationic peptides. Newer targets that have been suggested include the sphingolipids, protein translational machinery that targets myristoylation of proteins, and DNA topoisomerases. A more recent approach to drug discovery utilizes genomics to search for targets (genomic mining) that offer specificity and minimal toxicity. In this chapter, first we review the antifungal agents that are the currently used favorites in treatment. Secondly, experimental targets are discussed, and finally, genomic approaches are mentioned.


Chapter 10: Molecular Basis of Antifungal Resistance
Rajendra Prasad, Nivedita Gupta and Manisha Gaur

Abstract
Several human pathogenic fungi including Candida albicans and its related species become resistant to antifungals and, as a result, the resistance interferes with successful chemotherapy. The resistance of these pathogenic fungi is not restricted to the commonly used triazole compounds but is even encountered, though not often, with polyene derivatives as well. Research during past decade confirms that the antifungal resistance phenomenon resembles multidrug resistance (MDR), a common occurrence in cancer cells. Similar to human P-glycoprotein (P-gp /MDR1) that encodes a drug extrusion pump, many of the pathogenic fungi also have such efflux pump proteins. The result of transcriptional activation of these encoding genes and their over expression is a rapid efflux of a drug. As a result of enhanced efflux activity, the resistant fungal cell accumulates much less drug intracellularly and is able to tolerate and grow in presence of antifungals. It is now established that antifungal resistance in fungi is not restricted to a single mechanism but is rather a multifactorial phenomenon. This chapter focuses on some of the molecular mechanisms underlying antifungal resistance.


Chapter 11: Fungal Biofilms and Drug Resistance
Gordon Ramage and José L. López-Ribot

Abstract
After attachment to a surface, many fungi can produce biofilms, a mixture of cells that coexist as an organized community that is enveloped within an exopolymeric matrix. Biofilms represent a protective environment and thus biofilm formation carries important clinical consequences. Indeed, the majority of human infections are associated with biofilm formation. Candida albicans remains the fungal species most commonly associated with biofilm formation on both host tissues and medical devices. Mature C. albicans biofilms consist of a dense network of yeasts cells and filamentous elements embedded within a three-dimensional structure consisting of exopolymeric material, microcolonies, and water channels. Sessile fungal cells within the biofilm are resistant to a range of antifungal agents currently in clinical use, namely the triazoles and polyenes; the molecular basis of antifungal drug resistance in biofilms is multifactorial.


Chapter 12: Molecular Modelling of Echinocandin-Type Antibiotics Using Molecular Mechanics and Density Functional Theory Calculations
Juan Murgich, Héctor Franco and Gioconda San-Blas

Abstract
The search for new antifungals has recently focused upon drugs that may interfere with the synthesis of the fungal cell wall b-1,3-glucan, a structure unique to most human fungal pathogens. The specificity of these drugs should mean that they are less toxic than the currently available antifungals. Among these inhibitors, echinocandins are fungal secondary metabolites composed of a cyclic hexapeptide core with a lipid side chain that is responsible for antifungal activity. Three echinocandin derivatives are currently in clinical development, caspofungin, anidulafungin and micafungin. It is expected that properties such as electrostatic potential, dipole moment, and others will be important factors in determining the therapeutic action of these drugs. In this work, we have used a non-local density functional in the calculation of the stable molecular conformation in water, the molecular electrostatic potential, and related properties for each of the three echinocandins mentioned above. Molecular Mechanics calculations indicated that the side chain tail opposite the polypeptide ring in flat structural representations is adjacent to this ring in a low-energy 3D conformation. In each of the inhibitors, the electrostatic equipotential surface shows a complex and convoluted shape as a result of the presence of the highly electronegative atoms such as O and N in the polypeptides and in some of the tails.

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