A contractile vacuole complex is involved in osmoregulation in Trypanosoma cruzi

Abstract

Acidocalcisomes are dense, acidic organelles with a high concentration of phosphorus present as pyrophosphate and polyphosphate complexed with calcium and other cations. Acidocalcisomes have been linked to the contractile vacuole complex in Chlamydomonas reinhardtii, Dictyostelium discoideum, and Trypanosoma cruzi. A microtubule-and cyclic AMP-mediated fusion of acidocalcisomes to the contractile vacuole complex in T. cruzi results in translocation of aquaporin and the resulting water movement which, in addition to swelling of acidocalcisomes, is responsible for the volume reversal not accounted for by efflux of osmolytes. Polyphosphate hydrolysis occurs during hyposmotic stress, probably increasing the osmotic pressure of the contractile vacuole and facilitating water movement. Index DescriptorsChlamydomonas reinhardtii; Dictyostelium discoideum; Trypanosoma cruzi; Kinetoplastida; acidocalcisomes; contractile vacuole Need for osmoregulation in Trypanosoma cruziTrypanosoma cruzi has a complex life cycle involving several morphological and functionally different stages. As T. cruzi progresses through its life cycle, it encounters diverse environmental stressors to which it must successfully adapt. Of particular interest is the parasite's ability to cope with extreme fluctuations in osmolarity that occur within the gut of the vector (Kollien et al., 2001;Kollien and Schaub, 2002) and also as the parasite moves from the insect gut through the acidic phagolysosome to the cytosol of the host cell. The infective form of the parasite passes out of the vector in the highly concentrated excreta (600-700 mOsm) (Kollien et al., 2001) and rapidly encounters the interstitial fluid of the mammalian host with a much lower osmolarity (300 mOsm). Clearly the parasite must have mechanisms that allow it to adapt both to hyperosmotic and hyposmotic stresses. In this review we limit our discussion to the response of T. cruzi to hyposmotic stress. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access Adaptation to hyposmotic stress in vertebrate cellsPhysiological adaptations to hyposmotic stress have been studied extensively in a wide range of vertebrate cell types. Upon exposure to a reduction in external osmolarity, cells initially swell but soon regain nearly normal cell volume by a process that has been termed the Regulatory Volume Decrease (RVD; reviewed in (Lang et al., 1998a; Lang et al., 1998b), which is accomplished by the efflux of various inorganic ions (such as Na + and K + ) and organic osmolytes to the extracellular environment. Vertebrate cells maintain hig...

Rab32 is essential for maintaining functional acidocalcisomes, and for growth and infectivity of Trypanosoma cruzi

“…Fusion of acidocalcisomes with the contractile vacuole, and the concomitant hydrolysis of polyP has been postulated to lead to an increase in phosphate and cations in the bladder, resulting in water accumulation Rohloff and Docampo, 2008). These changes are likely to be accompanied by the transfer of a phosphate transporter and cation exchangers (Ulrich et al, 2011) from the acidocalcisome membranes, together with TcAQP1 , providing the means for water accumulation (through TcAQP1), as well as for the return of cations (cation exchangers) and phosphate (P i transporter) to the cytosol after water elimination .…”

Structural organization of Trypanosoma cruzi

“…These structures seem to be involved in process of osmoregulation. It has been shown that fusion of acidocalcisomes to the contractile vacuole takes place via a process mediated by cyclic adenosine monophosphate (Rohloff & Docampo 2008).…”

The SEC6 protein is required for function of the contractile vacuole inChlamydomonas reinhardtii

“…In addition, our knowledge of how the CV cycle is controlled and adapted to the need of the cell is at best fragmentary. Calcium, protein kinases and cAMP have been implicated (Rohloff and Docampo, 2008), but in no system is the CV really understood.…”