Changes in lipolysis and lipogenesis in selected tissues of the landlocked lamprey,Petromyzon marinus, during metamorphosis

Kao, Ying-Jer; Youson, John H.; Holmes, J. H. G.; Sheridan, Mark A.

doi:10.1002/(sici)1097-010x(19970301)277:4<301::aid-jez4>3.0.co;2-t

Cited by 23 publications

(9 citation statements)

References 18 publications

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“…This increase in spermiating males may facilitate the synthesis of a bile acid pheromone with secretion rate about 0.5 mg/h (35). Interestingly, lipolysis and fatty acid synthesis in liver and intestine vary significantly among life stages (36). Further examination of cholesterol homeostasis may elucidate the adaptive value of bile salt de novo synthesis in lamprey intestine.…”

Section: Resultsmentioning

confidence: 99%

Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey

Yeh

Chung-Davidson

Wang

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Bile salt synthesis is a specialized liver function in vertebrates. Bile salts play diverse roles in digestion and signaling, and their homeostasis is maintained by controlling input (biosynthesis) and intestinal conservation. Patients with biliary atresia (i.e., obliteration of the biliary tree) suffer liver fibrosis and cirrhosis. In contrast, sea lamprey thrives despite developmental biliary atresia. We discovered that the sea lamprey adapts to biliary atresia through a unique mechanism of de novo synthesis and secretion of bile salts in intestine after developmental biliary atresia, in addition to known mechanisms, such as the reduction of bile salt synthesis in liver. During and after developmental biliary atresia, expression of cyp7a1 in intestine increased by more than 100-fold ( P < 0.001), whereas in liver it decreased by the same magnitude ( P < 0.001). Concurrently, bile salt pools changed in similar patterns and magnitudes in these two organs and the composition shifted from C24 bile alcohol sulfates to taurine-conjugated C24 bile acids. In addition, both in vivo and ex vivo experiments showed that aductular sea lamprey secreted taurocholic acid into its intestinal lumen. Our results indicate that the sea lamprey, a jawless vertebrate, may be in an evolutionarily transitional state where bile salt synthesis occurs in both liver and intestine. Understanding the molecular basis of these mechanisms may shed light on the evolution of bile salt synthesis and possible therapy for infant biliary atresia.

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Section: Resultsmentioning

confidence: 99%

Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey

Yeh

Chung-Davidson

Wang

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…This size is greater than the minimum for premetamorphic sea lamprey larvae from the Great Lakes (≥120 mm (length) and ≥3.0 g (mass); Youson et al 1993), premetamorphic L. fluviatilis and L. planeri (Bird and Potter 1979b), and premetamorphic G. australis . If, as in sea lampreys, lipid is the primary source of energy during the nontrophic phase of metamorphosis (Lowe et al 1973;Kao et al 1997), then the large size of premetamorphic L. appendix larvae may reflect a requirement for larger energy reserves to sustain individuals during the nontrophic periods of metamorphosis and subsequent sexual maturation. However, it is not clear why L. appendix is so much larger (length and mass) than some other nonparasitic species (e.g., L. planeri) before, during, and after metamorphosis.…”

Section: Discussionmentioning

confidence: 97%

“…Kao et al (1997) found that spontaneous metamorphosis in sea lampreys was dominated by lipogenesis up to stage 3, and that the later stages were characterized by enhanced lipolysis and reduced lipogenesis and oxidative metabolism, relative to nonmetamorphosing larvae. If similar mechanisms are present in L. appendix, then metamorphosing animals may be better able than nonmetamorphosing larvae to cope with the energetic demands of metamorphosis and the higher than normal temperatures used in the present study.…”

Section: Discussionmentioning

confidence: 99%

“…Although Eales et al (1997) suggested that monodeiodinase pathways might have an important role in lamprey metamorphosis, recent data indicate that KClO 4 does not affect the T 4 outer ring deiodination pathway to T 3 in sea lampreys (Manzon et al 1998). Kao et al (1997) noted that a switch in lipid metabolism from lipogenesis to lipolysis, which occurs at stage 3, is a key event in sea lamprey metamorphosis. We suggest that KClO 4 may act directly on this pathway to induce metamorphosis in lampreys.…”

Section: Discussionmentioning

confidence: 99%

“…Because both metamorphosis and the subsequent period of sexual maturation are nontrophic in nonparasitic species, the larvae presumably have greater energy reserves prior to entering metamorphosis than those of parasitic species that feed between metamorphosis and spawning. If, as in sea lampreys, lipid is the primary energy store (Lowe et al 1973;Kao et al 1997), then animal size and condition might also be important requirements for metamorphosis in nonparasitic lampreys.…”

Section: Introductionmentioning

confidence: 99%

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Spontaneous and induced metamorphosis in the American brook lamprey, <i>Lampetra appendix</i>

Holmes¹,

Chu²,

Khanam³

et al. 1999

Can. J. Zool.

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Abstract:We described the seven stages of spontaneous metamorphosis in the American brook lamprey (Lampetra appendix) and assessed the importance of size as a determinant of spontaneous and induced metamorphosis. Serum concentrations of the thyroid hormones (TH) thyroxine (T 4 ) and triiodothyronine (T 3 ) were measured in metamorphosing and nonmetamorphosing L. appendix. The sequence of stages in metamorphosis and changes in the relative lengths of most body regions were consistent with data reported for other lamprey species. However, premetamorphic and metamorphosing L. appendix in the early stages of metamorphosis (1-3) were much larger in size (at least 155 mm and 5.40 g) than has been observed for other lamprey species. Serum concentrations of T 4 and T 3 were high by the end of the larval period and declined significantly by stage 2 of metamorphosis. Larvae ≥130 mm in length were treated with either potassium perchlorate (KClO 4 ; 0.01 and 0.05%) or 10 mg/L propylthiouracil (PTU; 0.0001%) for 117 days from September to January to determine if metamorphosis could be induced by these goitrogens. Both concentrations of KClO 4 successfully induced metamorphosis in L. appendix, but the incidence of metamorphosis (62%) was much lower than reported in sea lampreys (98%) of comparable size. Serum concentrations of T 4 and T 3 declined by 64-76 and 93-96% relative to control values, respectively, in metamorphosing and nonmetamorphosing L. appendix treated with KClO 4 . PTU elicited declines of 55% for T 4 and 80% for T 3 , but only one animal metamorphosed. Based on these data, we conclude that a decline in serum TH levels is necessary for metamorphosis in L. appendix, but not sufficient by itself to trigger the process.Résumé : On trouvera ici la description des sept stades de métamorphose spontanée chez la lamproie (Lampetra appendix); nous avons évalué l'importance de la taille comme facteur déterminant de la métamorphose spontanée et de la métamorphose provoquée. Les concentrations sériques des hormones thyroïdiennes (TH) thyroxine (T 4 ) et triiodothyronine (T 3 ) ont été mesurées chez des lamproies en métamorphose et chez d'autres lamproies non en métamorphose. La séquence des stades de métamorphose et les modifications de la longueur relative de la plupart des zones du corps correspondent aux données signalées pour d'autres espèces. Cependant, chez cette espèce, les lamproies prémétamorphiques et les lamproies en métamorphose au cours des premiers stades (1-3) sont de taille bien supérieure (au moins 155 mm et 5,40 g) à celle mesurée chez d'autres espèces. Les concentrations sériques de T 4 et de T 3 sont élevées à la fin de la période larvaire et diminuent considérablement jusqu'au stade 2 de la métamorphose. Nous avons administré du perchlorate de potassium (KClO 4 ; 0,01 et 0,05%) ou 10 mg/L de propylthiouracil (PTU; 0,0001%) à des larves de longueur ≥130 mm durant 117 jours, de septembre à janvier, afin de vérifier si ces goitrogènes peuvent provoquer la métamorphose chez les poissons. Les deux concentr...

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Expression of proopiocortin and proopiomelanotropin during the life cycle of the sea lamprey (Petromyzon marinus)

et al. 1999

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The sea lamprey shows an important divergence in the proopiomelanocorticotropin (POMC) prohormone in that adrenocorticotropin (ACTH) and melanocyte stimulating hormone (MSH) are encoded on distinct genes, proopiocortin (POC) and proopiomelanotropin (POM), respectively. POC encodes nasohypophysial factor (NHF), ACTH, and β-endorphin while POM encodes αand β-MSH-like peptides (called MSH-B and MSH-A, respectively), and a second form of β-endorphin. The present study examined the variation in expression of these two genes during the life cycle of sea lampreys. Individual Northern blot analysis and pooled data from several Northern blots showed significant differential expression of POC and POM during the lamprey life cycle. While POC expression remained low over larval and metamorphic stages, POM expression rose substantially in stage 4 and stage 6 of metamorphosis. Both POC and POM expression levels increased in immediately post-metamorphic animals. The highest levels of POM expression were observed in larger juvenile adults and pre-spawners, whereas the highest level of POC expression was observed at the prespawning period. Statistical analysis showed POM expression to be much higher than POC expression in immediately post-metamorphic animals prior to feeding. Northern analysis of total RNA isolated from various tissues in the pre-spawning lampreys, including brain, showed expression of POC and POM only in the pituitary. These observations indicate that the expression of POC and POM, which encode different sets of hormones, may be related to developmental and maturation events during the life cycle of the sea lamprey.

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Changes in lipolysis and lipogenesis in selected tissues of the landlocked lamprey,Petromyzon marinus, during metamorphosis

Cited by 23 publications

References 18 publications

Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey

Intestinal synthesis and secretion of bile salts as an adaptation to developmental biliary atresia in the sea lamprey

Spontaneous and induced metamorphosis in the American brook lamprey, <i>Lampetra appendix</i>

Expression of proopiocortin and proopiomelanotropin during the life cycle of the sea lamprey (Petromyzon marinus)

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