Lymphatic vessels in lungfishes (Dipnoi)

Vogel, W; Mattheus, Ulrich

doi:10.1007/s004350050045

Cited by 12 publications

(5 citation statements)

References 31 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…A more extensive SVS may be linked to increased scope for activity, which in turn may be associated with enhanced skin O 2 uptake via the SVS during exercise. There is no evidence of an SVS in lungfish (Vogel and Mattheus, 1998), but whether our Silurian vertebrate ancestors had a SVS subsequently lost in the Acanthodii or the SVS evolved in the Actinopterygii is unknown. What is clear is that the organization of circulation and requirements for fluid balance are different in aquatic and terrestrial vertebrates.…”

Section: Research Articlementioning

confidence: 99%

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Rummer

Wang

Steffensen

et al. 2013

Journal of Experimental Biology

View full text Add to dashboard Cite

Teleost fishes and mammalian lineages diverged 400 million years ago, and environmental requirements (water versus air) have resulted in marked differences in cardiovascular function between fish and mammals. Suggestions that the fish secondary vascular system (SVS) could be used as a model for the mammalian lymphatic system should be taken with caution. Despite molecular markers indicating similar genetic origin, functions of the SVS in teleost fish are probably different from those of the mammalian lymphatic system. We determined that, in resting glass catfish (Kryptopterus bicirrhis), plasma moves from the primary vascular system (PVS) to the SVS through small connecting vessels less than 10 μm in diameter, smaller than the red blood cells (RBCs). During and following hypoxia or exercise, flow increases and RBCs enter the SVS, possibly via β-adrenoreceptor-mediated dilation of the connecting vessels. The volume of the SVS can be large and, as RBCs flow into the SVS, the haematocrit of the PVS falls by as much as 50% of the resting value. Possible functions of the SVS, including skin respiration, ionic and osmotic buffering, and reductions in heart work and RBC turnover, are discussed. KEY WORDS: Lymphatic, Secondary vascular system, Stress INTRODUCTIONThe mammalian lymphatic system consists of blind-ending lymphatic vessels, lymph nodes and other tissues, including the spleen, that collect, filter and return fluid that drains from the tissues to the venous system and transport fats and proteins from the gut into the blood system (Alitalo et al., 2005;Wang and Oliver, 2010). In teleost fishes, some circulatory vessels contain clear fluid and have been described as lymphatic vessels (Kampmeier, 1969). Yaniv et al. (Yaniv et al., 2006) and Isogai et al. (Isogai et al., 2009) have also demonstrated that these vessels share some morphological and molecular characteristics with the lymphatic vessels found in other vertebrates, and suggested that these clear vessels in zebrafish could be used as a model for the mammalian lymphatic system. However, several decades ago these same vessels were hypothesized as part of a secondary vascular system (SVS), receiving inflow from the arterial system via arterio-arterial anastomoses and emptying into the venous circulation (Vogel, 1981;Vogel and Claviez, 1981;Vogel, 1985;Steffensen et al., 1986;Steffensen and Lomholt, 1992; RESEARCH ARTICLE Jensen et al., 2009). These vessels are not blind-ending and sometimes include red blood cells (RBCs) (Ishimatsu et al., 1992). Furthermore, there is no evidence that the SVS vessels are draining edematous tissues or are playing a role in lipid transport. If not lymphatic, what then is the role of this secondary vascular system?The volume of the SVS can range from 10-50% to nearly twice the volume of the primary circulation (Bushnell et al., 1998;Gallaugher and Farrell, 1998;Skov and Steffensen, 2003;Steffensen and Lomholt, 1992) and therefore may serve to buffer osmotic and ionic changes in the primary circulation. Under restin...

show abstract

Section: Research Articlementioning

confidence: 99%

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Rummer

Wang

Steffensen

et al. 2013

Journal of Experimental Biology

View full text Add to dashboard Cite

show abstract

“…This group appears to have the first recognizable tetrapod-like lymphatic system among the vertebrates. The lymphatic system of Dipnoi is characterized by the presence of lymphatic capillaries and a large number of lymphatic micropumps located throughout the body, except for the central nervous system (114). There are high concentrations of lymphatic micropumps in the fin regions, up to 100 mm Ϫ3 in the South American lungfish (Lepidosiren paradoxa).…”

Section: Lymphatic Function In Lungfishes and The Water-land Transitionmentioning

confidence: 99%

“…The lymphatic micropumps are fed by thin-walled afferent lymphatic vessels that have no direct connection with the primary circulation and contain valves at the inlet and outlet that are adjacent to a blood capillary, presumably to collect filtrate from the adjacent interstitial space. There was no evidence for the "secondary circulation" vessels characteristic of teleosts (114). No studies have examined lymphatic development, the rate of volume flux, nor measured the pressures within the lymphatic system in this key group of vertebrates.…”

Section: Lymphatic Function In Lungfishes and The Water-land Transitionmentioning

confidence: 99%

Lymphatic regulation in nonmammalian vertebrates

Hedrick

Hillman

Drewes

et al. 2013

Journal of Applied Physiology

View full text Add to dashboard Cite

All vertebrate animals share in common the production of lymph through net capillary filtration from their closed circulatory system into their tissues. The balance of forces responsible for net capillary filtration and lymph formation is described by the Starling equation, but additional factors such as vascular and interstitial compliance, which vary markedly among vertebrates, also have a significant impact on rates of lymph formation. Why vertebrates show extreme variability in rates of lymph formation and how nonmammalian vertebrates maintain plasma volume homeostasis is unclear. This gap hampers our understanding of the evolution of the lymphatic system and its interaction with the cardiovascular system. The evolutionary origin of the vertebrate lymphatic system is not clear, but recent advances suggest common developmental factors for lymphangiogenesis in teleost fishes, amphibians, and mammals with some significant changes in the water-land transition. The lymphatic system of anuran amphibians is characterized by large lymphatic sacs and two pairs of lymph hearts that return lymph into the venous circulation but no lymph vessels per se. The lymphatic systems of reptiles and some birds have lymph hearts, and both groups have extensive lymph vessels, but their functional role in both lymph movement and plasma volume homeostasis is almost completely unknown. The purpose of this review is to present an evolutionary perspective in how different vertebrates have solved the common problem of the inevitable formation of lymph from their closed circulatory systems and to point out the many gaps in our knowledge of this evolutionary progression.

show abstract

“…What is less well known is that in addition to the above recognized mechanisms facilitating lymph movement, the lymphatic system of many vertebrates acquires a specific contractile organ named the lymphatic heart [44][45][46][47][48][49][50][51][52][53][54][55][56][57]. It was documented by many investigations that the main structural component of lymphatic hearts is striated muscle cells [e.g., [45,46,48,[50][51][52]54], with only one report on smooth muscle morphology of the lymphatic heart [49].…”

Section: Implication #2mentioning

confidence: 99%

“…It was documented by many investigations that the main structural component of lymphatic hearts is striated muscle cells [e.g., [45,46,48,[50][51][52]54], with only one report on smooth muscle morphology of the lymphatic heart [49].…”

Section: Implication #2mentioning

confidence: 99%

Striated muscles in visceral organs of vertebrates

Субботин¹

2016

J Histol Histopathol

View full text Add to dashboard Cite

Pathologists involved in the examination of small rodent tissues are familiar with the presence of striated muscle in walls of intrapulmonary veins. Because these striated muscles express cardiomyocyte markers and are involved in rhythmical contraction during systole, this morphologic arrangement was named "pulmonary myocardium". Striated cardiac muscles of intrapulmonary veins have also been found in numerous species, including non-human primates. Great attention has been given to animal striated pulmonary veins because in humans, the presence of cardiomyocytes in the pulmonary veins (myocardial sleeves) is a major origin of paroxysmal atrial fibrillation. It is unequivocally suggested that direct extension/migration of cardiomyocytes from the left atrium into pulmonary veins is the origin of "pulmonary myocardium". This model sounds logical in regard to humans and large mammals because in these cases, striated myocytes extend into pulmonary veins only by 10-30 mm from the left atrium. However, the cardiomyocyte direct extension/migration model becomes less parsimonious when applied to the numerous small intrapulmonary veins with striated muscles in their walls in small mammals. In 1972, Alfred Sherwood Romer, renowned for his contributions to the study of vertebrate evolution, suggested that visceral smooth muscle cells developed a striated phenotype due to the need for more efficient musculature. Romer theorized that the primary anatomical division of the vertebrate muscular system should be not into smooth and striated types but into somatic and visceral systems, because the line of division along the gut between striated and smooth musculature is not a fixed point. Romer's work offered a parsimonious model for the presence of striated muscle in the walls of the intrapulmonary veins-visceral smooth muscle cells, which are capable of differentiating into striated muscle cells, are always present; whether they differentiate depends on functional demands. From Romer's hypothesis, it also could be foreseen that striated muscle could appear in visceral compartments other than the blood circulatory system and pharyngeal muscles to facilitate functional needs. Indeed, it was shown that 1) the lymphatic system of many low vertebrates acquired a lymphatic heart with striated muscle cells; 2) some vertebrates also acquire striated muscles in tunica Muscularis of the stomach and intestine. The facts above undoubtedly corroborate Prof. Romer's notion on the evolution of the vertebrate muscular system.

show abstract

Lymphatic vessels in lungfishes (Dipnoi)

Cited by 12 publications

References 31 publications

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Function and control of the fish secondary vascular system, a contrast to mammalian lymphatic systems

Lymphatic regulation in nonmammalian vertebrates

Striated muscles in visceral organs of vertebrates

Contact Info

Product

Resources

About