Functional integration of the circulatory, immune, and respiratory systems in mosquito larvae: pathogen killing in the hemocyte-rich tracheal tufts

League, Garrett P.; Hillyer, Julián F.

doi:10.1186/s12915-016-0305-y

Cited by 39 publications

(48 citation statements)

References 78 publications

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“…A recently described immune phenomenon in mosquitoes relies on sessile periosteal hemocytes attached to the periosteum region of the heart (i.e., flanking the valves) to sequester and concentrate circulating microbes and pathogens (King & Hillyer, ; League & Hillyer, ; Sigle & Hillyer, ). This builds on previous observations that pathogens accumulate in discrete foci along the surface of the mosquito heart during infection (Hillyer, Barreau & Vernick, ).…”

Section: Hemocyte Roles In Melanizationmentioning

confidence: 99%

Re‐evaluation of insect melanogenesis research: Views from the dark side

Whitten

Coates

2017

Pigment Cell Melanoma Res

105

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Summary Melanins (eumelanin and pheomelanin) are synthesized in insects for several purposes including cuticle sclerotization and color patterning, clot formation, organogenesis, and innate immunity. Traditional views of insect immunity detail the storage of pro‐phenoloxidases inside specialized blood cells (hemocytes) and their release upon recognition of foreign bodies. Activated phenoloxidases convert monophenols into reactive quinones in a two‐step enzymatic reaction, and until recently, the mechanism of tyrosine hydroxylation remained a mystery. Herein, we present our interpretations of these enzyme–substrate complexes. The resultant melanins are deposited onto the surface of microbes to immobilize, agglutinate, and suffocate them. Phenoloxidase activity and melanin production are not limited to the blood (hemolymph) or cuticle, as recent evidence points to more diverse, sophisticated interactions in the gut and with the resident symbionts. This review offers insight into the somewhat neglected areas of insect melanogenesis research, particularly in innate immunity, its role in beneficial insects such as pollinators, the functional versatility of phenoloxidases, and the limitations of common experimental approaches that may impede progress inadvertently.

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Section: Hemocyte Roles In Melanizationmentioning

confidence: 99%

Re‐evaluation of insect melanogenesis research: Views from the dark side

Whitten

Coates

2017

Pigment Cell Melanoma Res

105

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“…In adults, this is reflected in the aggregation of haemocytes at the periostial regions, which surround the locations where haemolymph enters the heart (King & Hillyer, ; Sigle & Hillyer, ). Haemolymph circulation in larvae is different, which is reflected by the aggregation of haemocytes at the tracheal tufts that surround the sole entry point for haemolymph into the larval heart (League et al ., ; League & Hillyer, ). Here, we expanded our understanding of the biology of periostial haemocytes, and implicate two Nimrod family genes – eater and draper – in periostial immune responses.…”

Section: Discussionmentioning

confidence: 99%

Eater and draper are involved in the periostial haemocyte immune response in the mosquito Anopheles gambiae

Sigle

Hillyer

2018

Insect Molecular Biology

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Haemocytes respond to infection by phagocytosing pathogens, producing the enzymes that drive the phenoloxidase-based melanization cascade, secreting lytic factors, and producing other humoral proteins. A subset of haemocytes, called periostial haemocytes, aggregate on the surface of the heart of mosquitoes and kill pathogens in areas of high haemolymph flow. Periostial haemocytes are always present, but an infection induces the recruitment of additional haemocytes to these regions. Here, we tested whether members of the Nimrod gene family are involved in the periostial immune response of the African malaria mosquito, Anopheles gambiae. Using organismal manipulations, RNA interference (RNAi) and microscopy, we show that, following an infection with Escherichia coli, nimrod - the orthologue of Drosophila NimB2 - is not involved in periostial responses. At 4 h postinfection, however, RNAi-based knockdown of draper results in a marginal increase in the number of periostial haemocytes and a doubling of E. coli accumulation at the periostial regions. Finally, at 24 h postinfection, knockdown of eater decreases the number of periostial haemocytes and decreases the phagocytosis of E. coli on the surface of the heart. Phagocytosis of bacteria is more prevalent in the periostial regions of the mid abdominal segments, and knockdown of draper, nimrod or eater does not alter this distribution. Finally, knockdown of Nimrod family genes did not have a meaningful effect on the accumulation of melanin at the periostial regions. This study identifies roles for eater and draper in the functional integration of the mosquito immune and circulatory systems.

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“…Metamorphosis involves considerable shifts in the ecology and physiology of many invertebrates, including alterations to the immune system (League, Estevez‐Lao, Yan, Garcia‐Lopez, & Hillyer, ; League & Hillyer, ; Russell & Dunn, ). In mosquitoes, metamorphosis has decoupled the larval and adult immune systems such that immunity is strongest in larvae and declines after eclosion and with adult age (League et al, ).…”

Section: Introductionmentioning

confidence: 99%

“…The aquatic habitats of mosquito larvae are rife with microorganisms that can invade the hemocoel (body cavity) (Bartholomay & Michel, ; Granados, ; Kalucy & Daniel, ; Petersen, Chapman, & Woodard, ; Sweeney, Inman, Bland, & Wright, ; Washburn, Egerter, Anderson, & Saunders, ; Yassine, Kamareddine, & Osta, ). Consequently, mosquito larvae mount powerful cellular and humoral immune responses against pathogens in their hemocoel (Biron et al, ; Dimopoulos, Richman, Muller, & Kafatos, ; Duncan et al, ; Kalucy & Daniel, ; League et al, ; League & Hillyer, ; Meredith, Hurd, Lehane, & Eggleston, ; Richman et al, ; Shin et al, ). Recently, we demonstrated that a larval‐acquired infection in the hemocoel is transstadially transmitted to the hemocoel of an adult, which may have important implications for adult immunity (Brown, Thompson, & Hillyer, ).…”

Section: Introductionmentioning

confidence: 99%

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

Brown

Shapiro

Thompson

et al. 2019

Ecology and Evolution

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Larval and adult mosquitoes mount immune responses against pathogens that invade their hemocoel. Although it has been suggested that a correlation exists between immune processes across insect life stages, the influence that an infection in the hemocoel of a larva has on the immune system of the eclosed adult remains unknown. Here, we used Anopheles gambiae to test whether a larval infection influences the adult response to a subsequent bacterial or malaria parasite infection. We found that for both female and male mosquitoes, a larval infection enhances the efficiency of bacterial clearance following a secondary infection in the hemocoel of adults. The adults that emerge from infected larvae have more hemocytes than adults that emerge from naive or injured larvae, and individual hemocytes have greater phagocytic activity. Furthermore, mRNA abundance of immune genes—such as cecropin A, Lysozyme C1, Stat‐A, and Tep1—is higher in adults that emerge from infected larvae. A larval infection, however, does not have a meaningful effect on the probability that female adults will survive a systemic bacterial infection, and increases the susceptibility of females to Plasmodium yoelii, as measured by oocyst prevalence and intensity in the midgut. Finally, immune proficiency varies by sex; females exhibit increased bacterial killing, have twice as many hemocytes, and more highly express immune genes. Together, these results show that a larval hemocoelic infection induces transstadial immune activation—possibly via transstadial immune priming—but that it confers both costs and benefits to the emerged adults.

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Functional integration of the circulatory, immune, and respiratory systems in mosquito larvae: pathogen killing in the hemocyte-rich tracheal tufts

Cited by 39 publications

References 78 publications

Re‐evaluation of insect melanogenesis research: Views from the dark side

Re‐evaluation of insect melanogenesis research: Views from the dark side

Eater and draper are involved in the periostial haemocyte immune response in the mosquito Anopheles gambiae

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

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