Mosquito Hemocytes Associate With Circulatory Structures That Support Intracardiac Retrograde Hemolymph Flow

Abstract

A powerful immune system protects mosquitoes from pathogens and influences their ability to transmit disease. The mosquito's immune and circulatory systems are functionally integrated, whereby intense immune processes occur in areas of high hemolymph flow. The primary circulatory organ of mosquitoes is the dorsal vessel, which consists of a thoracic aorta and an abdominal heart. In adults of the African malaria mosquito, Anopheles gambiae, the heart periodically alternates contraction direction, resulting in intracardiac hemolymph flowing toward the head (anterograde) and toward the posterior of the abdomen (retrograde). During anterograde contractions, hemolymph enters the dorsal vessel through ostia located in abdominal segments 2–7, and exits through an excurrent opening located in the head. During retrograde contractions, hemolymph enters the dorsal vessel through ostia located at the thoraco-abdominal junction, and exits through posterior excurrent openings located in the eighth abdominal segment. The ostia in abdominal segments 2 to 7—which function in anterograde intracardiac flow—are sites of intense immune activity, as a subset of hemocytes, called periostial hemocytes, respond to infection by aggregating, phagocytosing, and killing pathogens. Here, we assessed whether hemocytes are present and active at two sites important for retrograde intracardiac hemolymph flow: the thoraco-abdominal ostia and the posterior excurrent openings of the heart. We detected sessile hemocytes around both of these structures, and these hemocytes readily engage in phagocytosis. However, they are few in number and a bacterial infection does not induce the aggregation of additional hemocytes at these locations. Finally, we describe the process of hemocyte attachment and detachment to regions of the dorsal vessel involved in intracardiac retrograde flow.

Nitric oxide produced by periostial hemocytes modulates the bacterial infection induced reduction of the mosquito heart rate

“…Hearts were isolated by making an incision in the abdomen along the pleural membrane, removing the internal organs, and resecting the heart using 0.2 mm diameter minuten pins. Attached to these hearts are periostial hemocytes, pericardial cells and some alary muscles (Sigle and Hillyer, 2018a). The remainder of the abdomen is called the carcass and contains abdominal muscle, fat body, sessile hemocytes not associated with the heart, the ventral nerve cord, the integument and other cells that attach to the integument (Andereck et al, 2010;King and Hillyer, 2013).…”

“…In addition, we repeated this experiment but instead measured gene expression in the heart, the circulating hemocytes, the abdominal carcass and the whole body of mosquitoes that were naïve, injured or infected with E. coli for 1 day. Attached to the heart were the periostial hemocytes, pericardial cells and alary muscles (Sigle and Hillyer, 2018a), and attached to the abdominal carcass were the non-periostial sessile hemocytes (King and Hillyer, 2013). Many factors that affect heart rhythmicity have been identified in insects (Chowanśki et al, 2016;Hillyer, 2018), and here we focused on five genes encoding neuropeptides.…”

Adult Mosquitoes Infected with Bacteria Early in Life Have Stronger Antimicrobial Responses and More Hemocytes after Reinfection Later in Life

“…These sessile hemocytes adhere to many different tissues, and a specific population, called periostial hemocytes, adheres to the heart and actively phagocytoses pathogens as they flow toward the mosquito’s major circulatory organ [ 40 , 45 , 64 , 75 ]. Sessile hemocytes can become circulating and vice versa, and in D. melanogaster sessile hemocytes also function as a hematopoietic source of circulating hemocytes [ 64 , 76 , 77 , 78 , 79 ]. Whether an infection alters how sessile hemocytes respond to a second infection remains unknown.…”

Transstadial immune activation in a mosquito: Adults that emerge from infected larvae have stronger antibacterial activity in their hemocoel yet increased susceptibility to malaria infection

“…However, an adult infection results in an increase in the number of hemocytes in some mosquito species but not others (Coggins et al, ; Hillyer et al, ; King & Hillyer, ; League et al, ). When infection—or blood feeding—induces an increase, this is because of mitosis by circulating hemocytes, although sessile hemocytes may also release and enter circulation (Bryant & Michel, ; Castillo, Brown, & Strand, ; King & Hillyer, ; Sigle & Hillyer, , ). In the present study, we found that mosquitoes that receive both a larval infection and an infection as an adult have more hemocytes than those that were not infected as larvae.…”