Innervation regulates the metamorphic fates of larval abdominal muscles in the moth, Manduca sexta

Abstract

With the onset of metamorphosis, the abdominal muscles of the moth, Manduca sexta, follow one of three developmental fates: maintenance, respecification, or death. The maintained muscles retain their larval size and morphology throughout adult development. The respecified and dying muscles dedifferentiate, which involves regression, nuclear degeneration, and myofibril breakdown. Nuclei in both dying and respecified muscles also proliferate. The amount of nuclear degeneration is greater in the dying muscle fibers, and the amount of nuclear proliferation is greater in the respecified muscles. Four to ten days after pupation, the sizes of the respecified muscles stabilize while the dying muscles are lost. During regression, a subset of the respecified muscle fibers die. The surviving respecified muscle fibers grow and differentiate during the last half of adult development. In respecified muscles, denervation triggers an increased amount of nuclear degeneration and a decreased amount of nuclear proliferation. As a result, denervated respecified fibers experience increased muscle regression including an increased loss of muscle fibers and sometimes muscle death. Surviving respecified fibers still grow and differentiate yet are only 5 to 12% of the control size. Denervation triggers dedifferentiation in maintained muscles, resulting in fiber loss and occasionally muscle death. The percentage of fibers which dedifferentiate varies between different muscles. Denervation also triggers nuclear proliferation, with the amount of nuclear proliferation correlated with the extent of dedifferentiation of the individual muscle fibers. The dedifferentiated maintained fibers subsequently undergo differentiation in the absence of muscle growth.

Postembryonic development of the dorsal longitudinal flight muscle and its innervation inManduca sexta

“…4). The close spatial association between proliferating cells and the growing motor branches within the anlage suggests that the motoneurons may influence proliferation, as has been suggested for Drosophila (Currie and Bate, 1991;Fernandes and Keshishian, 1998) and for Manduca neuromuscular systems (Hegstrom and Truman, 1996;Luedeman and Levine, 1996;Bayline et al, 1998).…”

“…1; Nuesch, 1985), compared to abdominal body wall (cf. Tru-man and Reiss, 1995;Hegstrom and Truman, 1996;Bayline et al, 1998) or to thoracic leg muscles . Thus, a comparison of different muscle systems may provide insight into which developmental events, such as muscle degeneration, proliferation of myoblasts, or axonal and dendritic regression and outgrowth, are triggered synchronously by hormones in all systems and which are triggered independently, possibly by local factors.…”

“…The mechanisms underlying neuromuscular remodeling during metamorphosis involve hormonal signals (Weeks and Truman, 1985;Weeks and Levine, 1990;Prugh et al, 1992;Truman and Reiss, 1995;Hegstrom and Truman, 1996;Matheson and Levine, 1999) and cellular interactions (Kent and Levine, 1993;Bayline et al, 1998;Fernandes and Keshishian, 1998). The Manduca flight system offers several advantages for further investigation of these mechanisms.…”

Homeotic gene expression in the wild-type and a homeotic mutant of the moth Manduca sexta

“…3H). Based on the position and their orientation, the stained muscles appeared to be a subset of the internal muscles, including the dorsal intersegmental muscles, ventral lateral muscles, and ventral oblique muscles (Bayline et al 1998). We estimate that about half of the internal muscles located in A2 express Ubx.…”

Embryonic integument and “molts” in manduca sexta (insecta, lepidoptera)

“…The embryo of Manduca sexta has become a preferred model system to study pattern formation of an intermediate germ type (Booker and Truman, 1989;Carr and Taghert, 1989;Nagy et al, 1991;Miles and Booker, 1993;Kraft and Jä ckle, 1994;Patel, 1994;Warren et al, 1994;Sander, 1997;Zheng et al, 1999), the development of the nervous system (Taghert et al, 1988;Taghert, 1989a, b, 1991;Broadie et al, 1990;Westbrook and Bollenbacher, 1990;Westbrook et al, 1993), the evolution of endocrinological processes (Warren et al, 1986;Dorn et al, 1987b;Lanot et al, 1989;Dorn, 1998Dorn, , 2000, and morphogenetic processes (Nardi, 1993;Nardi and Cattani, 1995;Chen et al, 1997;Bayline et al, 1998). In order to allow a correlation of such studies, several attempts have been made to stage embryogenesis of M. sexta (Dorn et al, 1987a;Broadie et al, 1991;Dow et al, 1988).…”