Francine Marciano-Cabral, Ph.D.
Professor

Phone: (804) 828-9742
Dept. Fax: (804) 828-9946
e-mail: fmcabral@vcu.edu

Address:
Department of Microbiology & Immunology
Virginia Commonwealth University
P.O. Box 980678
1101 E. Marshall St., 7-058 Sanger Hall
Richmond, VA 23298-0678

Lab Web Page

Professional Experience

• B.S., 1966, College of White Plains 
• M.S., 1968, Villanova University
• Ph.D., 1973, University of Connecticut
• Postdoctoral, 1974-75, Baylor College of Medicine

Research Interests:

Naegleria Fowleri

The genus Naegleria consists of free-living amoebae widely distributed in soil and freshwater habitats throughout the world. Of the six species of Naegleria which have been identified in the environment, only one species, N. fowleri, has been associated with a fatal human infection. N. fowleri is the causative agent of primary amoebic meningoencephalitis, a rapidly fatal disease of the central nervous system.

The pathogenesis of this disease is poorly understood. Both weakly pathogenic and highly pathogenic strains of N. fowleri are known to exist. The pathogenicity of Naegleria amoebae in vivo correlates with resistance to complement-mediated lysis in vitro. Nonpathogenic Naegleria species activate the complement system and are readily lysed by complement. In contrast, highly pathogenic N. fowleri activate the complement pathway but are resistant to lysis. The ability of pathogenic amoebae to escape lysis by complement may be an important virulence factor in the pathogenesis of primary amoebic meningoencephalitis. The membrane attack complex of the complement system damages cell surface membranes by the formation of pores within the membrane of the target, resulting in lysis of the cell. A number of microorganisms and eucaryotic cells have developed mechanisms to evade complement lysis. Proteins which confer resistance to complement have been identified on the surface of pathogenic Naegleria . We have determined that enzymatic treatment of live amoebae with trypsin, papain, phosphatidylinositol-specific phospholipase C, and endoglycosidase H, to remove surface components, increases susceptibility of highly pathogenic amoebae to complement. The same enzymatic treatments of complement-sensitive nonpathogenic Naegleria have no effect on susceptibility of these amoebae to complement lysis. We are investigating the surface membrane components of complement resistant amoebae to identify the glycoproteins which play a role in protecting the amoebae from complement. We are determining whether HRF-like or CD59-like molecules are present on the surface of complement-resistant amoebae. In addition, we are determining whether other mechanisms of resistance play a role in protection. Another important factor which may contribute to the virulence of this organisms is its ability to detect neurochemicals. For example, highly pathogenic amoebae demonstrate chemotaxis for nerve cell factors but nonpathogenic amoebae do not. Thus, we are investigating the nerve cell factors which stimulate chemotaxis and may elicit directional migration to the brain in the host. We have produced C-DNA libraries to both highly pathogenic and nonpathogenic amoebae in order to investigate differences in the two strains and determine those characteristics which may allow a free-living amoeba to transform into a highly pathogenic virulent organism.

Selected Publications:

Cabral, G.A., Chairez, R., Marciano-Cabral, F., Suarez, M., Dreesman, G.R., Melnick, J.L., and F.B. Hollinger. 1975. Cell-mediated immunity in guinea pigs to subunits derived from hepatitis B surface antigen. Infect. Immun. 12: 564-570.

Fields, H., Dreesman, G., Hollinger, F., Marciano-Cabral, F., Gyorkey, F., and J. Melnick. 1976. Endogenous DNA polymerase-positive core particles from hepatitis-infected hepatocytes. Intervirology 6: 224-238.

Marciano-Cabral, F., Dix, R.D., Cabral, G.A., and R.J. Courtney. 1977. Effects of cytochalasin B on the maturation of herpes simplex virus type 1: An ultrastructural investigation. Virology 76: 860-865.

Marciano-Cabral, F. 1977. Intestinal and atrial flagellates and ciliates of man. In "Handbook Series in Clinical Laboratory Science: Microbiology Section." Seligson, D., and von Graevenitz, A., Eds. pp. 113-134. (CRC Press, Cleveland, Ohio)

Cabral, G.A., Marciano-Cabral, F., Funk, G., Hollinger, F., and G.R. Dreesman. 1978. Cell-mediated immunity to two polypeptides derived from hepatitis type B surface antigen. J. Gen. Virol. 38: 339-350.

Cabral, G.A., Courtney, R.J., Schaffer, P.A., and F. Marciano-Cabral. 1980. Ultrastructural characterization of an early large molecular weight nonstructural polypeptide of herpes simplex virus type 1. J. Virol. 33: 1192-1198.

Cabral, G.A., Marciano-Cabral, F., Patterson, M., Galen, E., and R. Carithers. 1981. Nuclear changes in hepatocytes from patients with non-A non-B hepatitis. Gastroenterology 81: 120-125.

Marciano-Cabral, F., Cabral, G.A., Miller, M., Patterson, M., and F. Farber. 1981. An autoradiographic study of the intracellular fate of infectious herpes simplex virus type 2 (HSV-2) DNA. Intervirology 16: 95-105.

Marciano-Cabral, F., Rublee, K.L., Carithers, R.L., Galen, E., Sobieski, T.J., and G.A. Cabral. 1981. Chronic non-A, non-B hepatitis: Ultrastructural and serologic studies. Hepatology 1: 575-582.

Patterson, M., Woodworth, T., Marciano-Cabral, F.M., and S.G. Bradley. 1981. Ultrastructure of enflagellation of Naegleria fowleri. J. of Bacteriol. 147: 217-226.

Marciano-Cabral, F. and S.G. Bradley. 1982. Cytopathogenicity of Naegleria gruberi for rat neuroblastoma cells. Infect. Immun. 35: 1139-1141.

Marciano-Cabral, F., Patterson, M., John, D., and S.G. Bradley. 1982. Cytopathogenicity of Naegleria fowleri and Naegleria gruberi for established mammalian cell cultures. J.of Parasitology 68: 1110-1116.

Cabral, G.A., Marciano-Cabral, F., Fry, D., Tomlin, H., Hall, D., and D. Gopelrud. 1982. Expression of herpes virus antigens in human premalignant and malignant cervical cells. In "Carcinoma of the cervix: Biology and Diagnosis" pp. 128-137, Martinez Nijoff Publ., Boston.

Cabral, G.A., Lumpkin, C., Fry, D., Mercer, L., Goplerud, D., and F. Marciano-Cabral. 1982. Expression of an herpesvirus antigen in premalignant and malignant human vulva cells. J. Obstet. & Gynecol. 143: 611-619.

Cabral, G.A., Fry, D., Marciano-Cabral,F., Lumpkin,C., Mercer,L., and D. Goplerud. 1983. A herpesvirus antigen in human premalignant and malignant cervical biopsies and explants. Am. J. Obstet. & Gynecol. 145: 79-86.

Reilly, M.F., Marciano-Cabral,F., Bradley, D.W. and S.G. Bradley. 1983. Agglutination of Naegleria fowleri and Naegleria gruberi by antibody in human serum. J. Clinical Microbiol 17: 576-581.

Marciano-Cabral, F., and D.T. John. 1983. Cytopathogenicity of Naegleria fowleri for rat neuroblastoma cell cultures:Scanning electron microscopy study. Infect. and Immun. 40:1214-1217.

Cline, M., Marciano-Cabral, F., and S.G. Bradley. 1983. Comparison of Naegleria fowleri and Naegleria gruberi cultivated in the same nutrient media. J. Protozool. 30: 387-391.

John, D.T., Cole, T.B., and F. Marciano-Cabral. 1984. Sucker-like structures on the pathogenic amoebae Naegleria fowleri. Appl. and Environmental Microbiol. 47: 12-14.

Morahan, P.S., Bradley, S.G., Munson, A.E., Duke, S., Fromtling, R.A. and F.M. Marciano-Cabral. 1984. Immunotoxic effects of diethylstilbestrol on host resistance: Comparison with cyclophosphamide. J. Leucocyte Biol. 35: 329-341.

Morahan, P.S., Bradley, S.G., Munson, A.E., Duke, S., Fromtling, R.A., and F. Marciano-Cabral. 1984. Immunotox effects of Diethylstilbestrol (DES) and Cadmium Chloride (CAD) on Host Resistance: Comparison with cyclophosphamide (CPS). Chemical Regulation of Immunity in Veterinary Medicine. pp. 403-406, Alan R. Liss, Inc., New York, N.Y.

Fulford, D.E., Bradley, S.G., and F. Marciano-Cabral. 1985. Cytopathogenicity of Naegleria fowleri for cultured rat neuroblastoma cells. J. Protozool. 32: 176-181.

Lattyak, M., Cabral,G. and F. Marciano-Cabral. 1985. Scanning electron microscopy of trophozoites of Naegleria species. Proc. Elect. Micros. Soc. Amer. 43: 642-643.

Cleary, S.F. and F. Marciano-Cabral. 1986. Activated macrophages demonstrate direct cytotoxicity, antibody-dependent cellular cytotoxicity and enhanced binding of Naegleria fowleri amoebae. Cellular. Immunol. 98: 125-136.

Cline, M., Carchman, R. and F. Marciano-Cabral. 1986. Stimulated movement of Naegleria by nerve cells. J. Protozool. 33: 10-13.

Marciano-Cabral, F. and D.E. Fulford. 1986. Cytopathology of pathogenic and nonpathogenic Naegleria species for cultured rat neuroblastoma cells. Appl. and Environ. Microbiol. 51: 1133-1137.

Cabral, G.A., Mishkin, E.M., Marciano-Cabral, F., Harris, L.S., Coleman, P. H., and A.E. Munson. 1986. Delta-9-Tetrahydrocannabinol decreases host resistance to Herpes simplex virus type 2 vaginal infections in the guinea pig. Proc. Exptl. Biol. Med. 182: 181-186.

Cleary, S.F. and F. Marciano-Cabral. 1986. Oxygen-independent killing of an extracellular protozoan, Naegleria fowleri by activated macrophages. Cellular Immunol. 101: 62-71.

Fulford, D. E. and F. Marciano-Cabral. 1986. Cytolytic activity of Naegleria fowleri cell-free extract. J. Protozool. 33: 498-502.

Marciano-Cabral, F. and M. Cline. 1987. Chemotaxis of Naegleria for bacteria. J. Protozool. 34: 127-131.

Marciano-Cabral, F., Cline, M. and S.G. Bradley. 1987. Specificity of antibodies from human serum for species of the amoeboflagellate, Naegleria. J. Clin. Microbiol. 25:692-697.

Marciano-Cabral, F., Stanitski, S., Radhakrishna, V., and S.G., Bradley. 1987. Characterization of a neutral aminoacyl-peptide hydrolase from Naegleria fowleri. J. Protozool. 34: 146-149.

Whiteman, L.Y., and F. Marciano-Cabral. 1987. Susceptibility of pathogenic and nonpathogenic Naegleria spp. to complement-mediated lysis. Infect. Immun. 55: 2442-2447.

Marciano-Cabral, F. 1988. The biology of Naegleria spp. Microbiological Reviews. 52: 114-133.

Zhang, L., Marciano-Cabral, F. and S. G. Bradley. 1988. Effects of cyclophosphamide and a metabolite, acrolein, on Naegleria fowleri in vitro and in vivo. Antimicrob. Agts. and Chemotherapy 32: 962-965.

Whiteman, L.Y. and F. Marciano-Cabral. 1989. Resistance of highly pathogenic Naegleria fowleri amebae to complement-mediated lysis. Infect. Immun. 57: 3869-3875.

Marciano-Cabral, F., Zoghby, K. and S. G. Bradley. 1990. Cytopathic action of Naegleria fowleri amebae on rat neuroblastoma cells. J. Protozool. 37: 138-144.

Fischer-Stenger, K., Cabral, G. A. and F. Marciano-Cabral. 1990. The interaction of Naegleria fowleri amebae with murine macrophage cell lines. J. Protozool. 37: 168-173.

Fischer-Stenger, K., Cabral, G. A. and F. Marciano-Cabral. 1992. Separation of soluble amebicidal and tumoricidal activity of activated macrophages. J. Protozool. 39: 235-241.

Brinkley, C. and F. Marciano-Cabral. 1992. A method for assessing the migratory response of Naegleria fowleri utilizing [3H] uridine-labeled amebae. J. Protozool. 39: 297-303.

Toney, D. and F. Marciano-Cabral. 1992. Alterations in protein expression and complement resistance of pathogenic Naegleria amebae. Infect. and Immun. 60: 2784-2790.

Fischer-Stenger, K. and F. Marciano-Cabral. 1992. The arginine-dependent cytolytic mechanism plays a role in destruction of Naegleria fowleri amebae by activated macrophages. Infect. Immun. 60:5126-5131.

Burnette-Curley, D., Marciano-Cabral, F., Fischer-Stenger, K. and G. A. Cabral. 1993. Delta-9-Tetrahycrocannabinol inhibits cell contact-dependent cytotoxicity of BCG-activated macrophages. Internat. J. Immunopharmacol. 15:371-382.

Marciano-Cabral, F. and D. Toney. 1994. Modulation of biological functions of Naegleria fowleri amebae by growth medium. J. Eukaryotic Microbiol. 41:38-46.

Toney, D. and F. Marciano-Cabral. 1994. Modulation of complement resistance of highly-pathogenic Naegleria fowleri by growth medium. J. Euk. Micro. 41:337-343.

Toney, D. and F. Marciano-Cabral. 1994. Membrane vesiculation of Naegleria fowleri amebae as a mechanism for resisting complement damage. J. Immunol. 152:2952-2959.

Petri, Jr., W. A. and F. Marciano-Cabral. 1994. Free-living Amoebae. In: Principles and Practice of Infectious Diseases, Ed. Mandell, G. L., Douglas, R.G., and J. E. Bennett. Fourth Edition. Churchill Livingstone, New York.

Bradley, S. G. and F. Marciano-Cabral. 1995. Antiparasitic Drugs. In: Principles of Pharmacology: Basic Concepts and Clinical Applications, Ed. Munson, P., Mueller and G. Breese. First Edition. Chapman and Hall, New York.

Wessberg, K.L., Skolnick, S., Xu, J., Marciano-Cabral, F., and R. G. Kemp. 1995. Cloning, sequencing, and expression of the pyrophosphate-dependent phosphofructo-1-kinase from Naegleria fowleri . Biochemical Journal 307:143-149.

Cabral, G.A., D. Toney, K. Fischer-Stenger and F. Marciano-Cabral. 1995.
Anandamide inhibits macrophage-mediated killing of tumor necrosis factor- sensitive cells. Life Sciences J. 56:2065-2073.

Dove Pettit, D. J. Williamson, G. A. Cabral and F.Marciano-Cabral.1996.In vitro destruction of nerve cell cultures by Acanthamoeba spp .: A transmission and scanning electron microscopy study. J. Parasitology 82:769-777.

Bradley, S. G., D.M. Toney, Y. J. Zhang and F. Marciano-Cabral. 1996. Dependence of growth, metabolic expression and pathogenicity of Naegleria fowleri on exogenous porphyrins. J. Parasitology 82:763-768.

Bradley, S. G. and F. Marciano-Cabral. 1996. Diversity of free-living ameboid organisms. J. Industrial Microbiology 17:314-321.

Toney, D. and F. Marciano-Cabral. 1998. Resistance of Acanthamoeba spp . to complement-mediated lysis. J. Parasitology 84:338-344.

Marciano-Cabral, F and D. Toney. 1998. The interaction of Acanthamoeb spp . with activated macrophages and with macrophage cell lines. J. Eukaryotic Microbiol. 45:452-458.

Chu DM, Miles H, Toney D. Ngyuen C, Marciano-Cabral F. 1998. Amebicidal activity of plant extracts from Southeast Asia on Acanthamoeba spp. Parasitol Res. 84(9):746-52.

Marciano-Cabral F, Puffenbarger R, Cabral GA. 2000. The increasing importance of Acanthamoeba infections. J Eukaryot Microbiology. 47(1):29-36.

Chu DM, Ferguson TJ, Marciano-Cabral F. 2000. Protein kinase activation and protein phosphorylation in Naegleria fowleri amebae in response to normal human serum. J Eukaryot Microbiology. 47(1):40-7.

Reveiller FL, Marciano-Cabral F, Pernin P, Cabanes PA, Legastelois S. 2000. Species specificity of a monoclonal antibody produced to Naegleria fowleri and partial characteriztaion of its antigenic determinant. Parasitol Res. 86(8):634-41.

Barbour SE, Marciano-Cabral F. 2001. Naegleria fowleri amoebae express a membrane-associated calcium-independent phospholipase A (2). Biochim Biophys Acta. 1530(2-3):123-33.

Carlisle SJ, Marciano-Cabral F, Staab A, Ludwick C, Cabral GA. 2002. Differential expression of the CB2 cannabinoid receptor by rodent macrophages and macrophage- like cells in relation to cell activation. Int Immunopharmacol. (1):69-82.

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